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A survey of xerophilic Aspergillus from indoor environment, including descriptions oftwo new section Aspergillus species producing eurotium-like sexual states
Visagie, Cobus M.; Yilmaz, Neriman; Renaud, Justin B.; Sumarah, Mark W.; Hubka, Vit; Frisvad, JensChristian; Chen, Amanda J.; Meijer, Martin; Seifert, Keith A.
Published in:MycoKeys
Link to article, DOI:10.3897/mycokeys.19.11161
Publication date:2017
Document VersionPublisher's PDF, also known as Version of record
Link back to DTU Orbit
Citation (APA):Visagie, C. M., Yilmaz, N., Renaud, J. B., Sumarah, M. W., Hubka, V., Frisvad, J. C., Chen, A. J., Meijer, M., &Seifert, K. A. (2017). A survey of xerophilic Aspergillus from indoor environment, including descriptions of twonew section Aspergillus species producing eurotium-like sexual states. MycoKeys, 19, 1-30.https://doi.org/10.3897/mycokeys.19.11161
A survey of xerophilic Aspergillus from indoor environment... 1
A survey of xerophilic Aspergillus from indoor environment, including descriptions of two new section Aspergillus species producing eurotium-like sexual states
Cobus M. Visagie1,2, Neriman Yilmaz1,2, Justin B. Renaud3, Mark W. Sumarah3, Vit Hubka4, Jens C. Frisvad5, Amanda J. Chen6,7, Martin Meijer6, Keith A. Seifert1,2
1 Department of Biology, University of Ottawa, 30 Marie-Curie, Ottawa, ON, Canada, K1N 6N5 2 Biodi-versity (Mycology), Agriculture and Agri-Food Canada, 960 Carling Avenue, Ottawa, ON, Canada, K1A 0C6 3 London Research & Development Centre, Agriculture & Agri-Food Canada, London, Ontario, N5V 4T3, Canada 4 Department of Botany, Faculty of Science, Charles University, Benátská 2, 128 01 Praque 2, Czech Republic 5 Department of Systems Biology, Building 221, Technical University of Denmark, DK-2800 Kgs. Lyngby, Denmark 6 Applied and Industrial Mycology, CBS-KNAW Fungal Biodiversity Centre, 8 Uppsalalaan, Utrecht, the Netherlands, 3584 CT 7 Institute of Medicinal Plant Development, Chinese Academy of medical Sciences and Peking Union Medical College, Beijing 100193, P.R. China
Corresponding author: Cobus M. Visagie (cobusvisagie9@gmail.com)
Academic editor: C. Gueidan | Received 11 November 2016 | Accepted 19 December 2016 | Published 9 January 2017
Citation: Visagie CM, Yilmaz N, Renaud JB, Sumarah MW, Hubka V, Frisvad JC, Chen AJ, Meijer M, Seifert KA (2017) A survey of xerophilic Aspergillus from indoor environment, including descriptions of two new section Aspergillus species producing eurotium-like sexual states. MycoKeys 19: 1–30. https://doi.org/10.3897/mycokeys.19.11161
AbstractXerophilic fungi grow at low water activity or low equilibrium relative humidity and are an important part of the indoor fungal community, of which Aspergillus is one of the dominant genera. A survey of xerophilic fungi isolated from Canadian and Hawaiian house dust resulted in the isolation of 1039 strains; 296 strains belong to Aspergillus and represented 37 species. Reference sequences were generated for all species and deposited in GenBank. Aspergillus sect. Aspergillus (formerly called Eurotium) was one of the most pre-dominant groups from house dust with nine species identified. Additional cultures deposited as Eurotium were received from the Canadian Collection of Fungal Cultures and were also re-identified during this study. Among all strains, two species were found to be new and are introduced here as A. mallochii and A. megasporus. Phylogenetic comparisons with other species of section Aspergillus were made using sequences of ITS, β-tubulin, calmodulin and RNA polymerase II second largest subunit. Morphological observa-tions were made from cultures grown under standardized conditions. Aspergillus mallochii does not grow at 37 °C and produces roughened ascospores with incomplete equatorial furrows. Aspergillus megasporus produces large conidia (up to 12 µm diam) and roughened ascospores with equatorial furrows. Echinulin, quinolactacin A1 & A2, preechinulin and neoechinulin A & B were detected as major extrolites of A. mega-sporus, while neoechinulin A & B and isoechinulin A, B & C were the major extrolites from A. mallochii.
Copyright Cobus M. Visagie et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
MycoKeys 19: 1–30 (2017)
doi: 10.3897/mycokeys.19.11161
http://mycokeys.pensoft.net
A peer-reviewed open-access journal
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RESEARCH ARTICLE
Cobus M. Visagie et al. / MycoKeys 19: 1–30 (2017)2
Key wordsBenA, CaM, indoor environments, mycotoxin, RPB2
Introduction
Species of Aspergillus section Aspergillus, the “A. glaucus” group of Thom and Raper (1941) and Raper and Fennell (1965), typically produce yellow cleistothecia (white in A. leucocarpus) with lenticular ascospores and the section includes species that were traditionally classified in the genus Eurotium. Species of section Aspergillus have a broad distribution in nature, but their xerophilic physiology makes them significant for the built environment and the food industry. In the built environment, species of section Aspergillus are among the primary colonizers of building materials (Flan-nigan and Miller 2011). Modern heating systems are designed to remove humidity from buildings, creating opportunities for xerophiles to dominate indoor fungal com-munities. Also of concern is the growth of these fungi in museums or libraries on historic artefacts such as books, carpets or paintings. They also commonly grow on/in leather, dust, softwood, a variety of textiles and even dried specimens in herbaria (Cavka et al. 2010; Micheluz et al. 2015; Pinar et al. 2013; Pinar et al. 2015; Pitt and Hocking 2009; Raper and Fennell 1965; Samson et al. 2010). For the food industry, these species have an economic impact because they can grow on stored grain, cereals or preserved foods with high sugar (i.e. jams, maple syrup) or salt content (i.e. biltong, dried fish) (Pitt and Hocking 2009; Samson et al. 2010).
Xerophily is a common physiological property of many Aspergillus species from several subgenera and sections, enabling those species to grow at low water activity (aw) or equilibrium relative humidity (ERH) (Flannigan and Miller 2011; Pitt 1975). Water activity is a measure of available water in liquid or solid substrates that has a significant effect on which organisms can grow on foods or other matrices, including building materials (Scott 1957). Reducing aw is widely used in the food industry to re-duce spoilage (Pitt and Hocking 2009). For the built environment, however, it is very difficult and often impractical to measure aw and as a result relative humidity (RH) is often used as a proxy. Because RH measures moisture in air rather than available water in a substrate, it is not considered a reliable indication of whether growth will actually occur on surfaces in the built environment (Flannigan and Miller 2011). A better measure is ERH because it is more representative of available water and is numerically proportional to aw (Flannigan and Miller 2011; Pitt and Hocking 2009).
Species of section Aspergillus produce many extrolites exhibiting a wide range of biological activities (Frisvad and Larsen 2015a; Gomes et al. 2012; Kanokmed-hakul et al. 2011; Li et al. 2008a; Li et al. 2008b; Slack et al. 2009; Smetani-na et al. 2007). Most notably, compounds from A. chevalieri were shown to be active against Plasmodium falciparum (malaria), Mycobacterium tuberculosis and cancer cell lines (Kanokmedhakul et al. 2011), an antitumor compound was reported from A. cristatus
A survey of xerophilic Aspergillus from indoor environment... 3
(Almeida et al. 2010), while many compounds are known to be antioxidants. They also produce mycotoxins, especially echinulin, flavoglaucin and physcion, which are toxic to animals (Ali et al. 1989; Bachmann et al. 1979; Cole and Cox 1981; Greco et al. 2015; Nazar et al. 1984; Rabie et al. 1964; Semeniuk et al. 1971; Slack et al. 2009; Ve-sonder et al. 1988), but toxicity has not been reported in humans. These species are not considered significant human pathogens, because most infections are superficial, with few cases of invasive infections known (de Hoog et al. 2014). Species commonly grow as saprobes on clinical specimens, such as skin and nails (Hubka et al. 2012). The biggest concern to humans, or nuisance, is the growth of these species inside homes, where exposure to spores and fragments, which contains β-(1, 3)-D-glucan, and other metabolites, cause allergies (Green et al. 2006; Slack et al. 2009).
Xerophilic fungi are well studied from a morphological point of view, but much work remains to develop reference sequence data for them. In this paper, we report on the diversity of Aspergillus isolated from house dust using media with low aw that select for the growth of xerophiles. Reference sequences are released for all species, in-cluding those received as Eurotium from the Canadian Collection of Fungal Cultures and re-identified here. Furthermore, we describe two new species and report on their extrolite production.
Materials and methods
Strains/sampling and isolations
House dust samples were received from various areas in North America. A modified dilution-to-extinction method (Collado et al. 2007) was used to isolate cultures, as de-scribed in Visagie et al. (2014a). Modifications included the use of 48-well titre plates rather than 96-well microtube plates and the use of Dichloran 18% Glycerol agar (DG18; (Hocking and Pitt 1980)), Malt extract yeast extract 10% glucose 12% NaCl agar (MY10-12) and Malt extract yeast extract 50% glucose agar (MY50G) (Sam-son et al. 2010) isolation media to select for xerophilic fungi.
In addition to newly obtained house dust isolates, several strains, including uni-dentified isolates and some reference or ex-type cultures, of Aspergillus sect. Aspergillus were obtained from the Canadian Collection of Fungal Cultures, Canada (DAOMC) and the CBS-KNAW Fungal Biodiversity Centre, the Netherlands (CBS).
Morphology
Colony characters were recorded from cultures grown for 7 d on various media, includ-ing CYA (Czapek yeast autolysate agar), MEA (Blakeslee’s malt extract agar), CREA (Creatine sucrose agar), CY20S (CYA with 20% sucrose agar), MEA20S (MEA with
Cobus M. Visagie et al. / MycoKeys 19: 1–30 (2017)4
20% sucrose agar), DG18, YES (yeast extract sucrose agar), M40Y (Harrold’s agar; 2% malt, 0.5% yeast extract, 40% sucrose), MY50G and MY10-12 (Harrold 1950; Pitt and Hocking 2009; Samson et al. 2014). Plates were incubated upside down in the dark at 25 °C and left unwrapped. Additional CY20S, DG18 and MEA20S plates were wrapped and incubated at 37 °C. Colour names and codes in descriptions are from Kornerup and Wanscher (1967). Microscopic preparations were made from colonies growing on DG18 and observations made using an Olympus SZX12 dissecting and Olympus BX50 compound microscopes equipped with Infinity3 and InfinityX cameras using Infinity Analyze v. 6.5.1 software (Lumenera Corp., Ottawa, Canada). Variation of conidia and ascospores was evaluated by measuring at least 50 structures and pre-sented as mean +/- standard deviation. Photographic plates were prepared in Pixelma-tor iOS v. 2.3 (http://www.pixelmator.com/ios), with photomicrographs modified for aesthetic purposes using the repair tool, without altering scientifically significant areas.
DNA extraction, sequencing and phylogenetic analysis
DNA was extracted from 8–10 d old colonies grown on DG18 using the UltracleanTM Microbial DNA isolation Kit (MoBio Laboratories Inc., Solana Beach, USA). Loci chosen for amplification included ITS barcodes (internal transcribed spacer rDNA region, in-cluding ITS1-5.8S-ITS2) (Schoch et al. 2012), BenA (partial β-tubulin), CaM (partial calmodulin) and RPB2 (RNA polymerase II second largest subunit). Thermocycler pro-grams used for amplification followed Samson et al. (2014) and employed primer pairs V9G & LS266 (ITS; (de Hoog and Gerrits van den Ende 1998; Masclaux et al. 1995), Bt2a & Bt2b (BenA; (Glass and Donaldson 1995)), CF1 & CF4 or sometimes CMD5 & CMD6 (CaM; (Hong et al. 2006; Peterson et al. 2005)) and 5F & 7CR (RPB2; (Liu et al. 1999)). Sequencing was done as described in Visagie et al. (2016). Contigs were assembled in Geneious v. 8.1.8 (Biomatters Ltd, New Zealand) and newly generat-ed sequences submitted to GenBank.
As a preliminary step in identification, CaM sequences derived from the newly isolated cultures were compared to an ex-type reference sequence database published by Samson et al. (2014). Then, gene sequences of the two presumed to be new sect. Aspergillus species were compared to reference datasets obtained from Peterson (2008), Hubka et al. (2013) and Visagie et al. (2014a). All datasets were aligned in MAFFT v. 7.221 (Katoh and Standley 2013) using the L-INS-i option for ITS and G-INS-i op-tion for the other genes. All alignments were trimmed in Geneious and then analysed as single and concatenated datasets using Maximum Parsimony (MP) and Bayesian In-ference of phylogenetic trees (BI). For concatenated phylogenies, a partitioned dataset of ITS, BenA, CaM and RPB2 regions was used.
MP analyses were run in PAUP* v. 4.0b10 (Swofford 2002) using heuristic searches with 100 random taxon additions and gaps treated as missing data. Support in nodes was calculated using a bootstrap analysis with the heuristic search option and 1000 replicates.
A survey of xerophilic Aspergillus from indoor environment... 5
BI analyses were run in MrBayes v. 3.2.5 (Ronquist et al. 2012). Model selections for BI were made for each gene based on the lowest Akaike Information Criterion (AIC) value, calculated in MrModeltest v. 2.3 (Nylander 2004). Analyses were run with two sets of four chains and stopped at a split frequency of 0.01. The sample fre-quency was set at 100 and 25 percent of trees removed as burnin. Trees were visualized in FigTree v. 1.4.2 (http://tree.bio.ed.ac.uk/software/figtree/) and prepared for pub-lication in Adobe® Illustrator® CS6. Aligned datasets, command blocks and trees were uploaded to TreeBase (www.treebase.org) under submission number 19771.
Extrolite analysis
For extrolite analysis, all strains were grown on 9 cm polystyrene Petri dishes on MEA supplemented with 7.5% NaCl at 25 °C for 14 d. Six agar plugs from each fungal isolate were removed with a sterilized 7 mm cork borer and placed into a 13 mL poly-propylene tube. Ethyl acetate (2 mL) was added to the tubes and vortexed for 30 s, followed by 1 h of sonication at 30 °C and vortexed again for 30 s. The supernatants were transferred into clean polypropylene tubes and dried on a centrifugal vacuum concentrator at 35° C. Extracts were reconstituted in 1 mL of 8:2 methanol:water and filtered into 2 mL amber glass HPLC vials using a 0.45 µm PVDF syringe filter. Ex-tracts were immediately stored at -20 °C until LC-MS analysis. Extracts were analyzed on a Q-Exactive orbitrap coupled to a 1290 Agilent HPLC in both positive and nega-tive polarities. Chemical formula of observed extrolites were determined with Xcalibur® software using accurate mass measurements and manually verified by isotopic pattern. Chemical formulae were searched against AntiBase2013 and Scifinder and putatively confirmed by comparing product ions observed with those published in the literature or though manual interpretation. The fungi were also analysed using the HPLC-DAD method described by Frisvad and Thrane (1987) as modified by Nielsen et al. (2011), by taking two agar plugs from each of the following media: DG18, CYA20S and YES agar, and extracting the combined 6 agar plugs of the colonies of Aspergillus with ethy-lacetate / isopropanol (3:1, vol./vol.) with 1% (vol.) formic acid added to that mixture. The retention indices and UV spectra were compared to those given in the supplemen-tary material of the Nielsen et al. (2011) paper.
Results
Sampling, isolations and identification
Isolations from house dust collected in Canada and Hawaii resulted in 1039 isolates of xerophilic/xerotolerant fungi. 296 isolates were identified as Aspergillus, of which mem-bers from sections Aspergillus, Nidulantes (A. versicolor clade) and Restricti were most
Cobus M. Visagie et al. / MycoKeys 19: 1–30 (2017)6
abundant. Strains were identified to species using CaM sequences and identities con-firmed by morphological examination. They include A. chevalieri, A. cibarius, A. monte-vidensis, A. proliferans, A. pseudoglaucus, A. ruber and A. tonophilus from sect. Aspergillus. In section Nidulantes (A. versicolor clade), A. jensenii and A. sydowii were isolated most frequently, while A. creber, A. fructus, A. protuberus, A. tenneseensis and A. versicolor were also recovered. A large degree of sequence diversity was observed in sect. Restricti and will be presented in a separate study. Other Aspergillus species identified include A. aureolatus, A. candidus, A. calidoustus, A. flavus, A. japonicus, A. lentulus, A. luchuensis, A. micro-nesiensis, A. niger, A. pragensis, A. tamarii, A. terreus, A. tubingensis, A. welwitschiae and A. westerdijkiae. Reference sequences, mostly CaM, obtained for these species were up-loaded to GenBank under accession numbers KX894565–KX894666 and KY351765–KY351785, and are included in Suppl. material 1: Table 1 to assist with future identi-fications. This table also include additional information with regard to strains’ location and growth medium used for their isolations. During this survey, two sect. Aspergillus species with eurotium-like sexual states could not be identified as known species and are described below as new species, based on growth characters on a wide range of culture media. The new species are compared with their close relatives and notes are provided on their diagnostic phenotypic characters, including extrolite production.
Phylogeny
To demonstrate genealogical concordance for the two new species, phylogenies for all known species of sect. Aspergillus were prepared (Table 1) using alignments of ITS, BenA, CaM, and RPB2 (Fig. 1) and overall phylogenetic relationships considered as a concatenated dataset (Fig. 2).
The ITS alignment was 535 bp long and contained 68 variable characters, of which 27 were parsimony informative. MP analysis resulted in two equally parsimonious trees (length 79 steps, CI = 0.987, RI = 0.992). HKY+I was found to be the most suit-able model for BI analysis. ITS is highly conserved in sect. Aspergillus, as demonstrated in the phylogenetic analysis, making it uninformative as an identification barcode in section Aspergillus. Of the 22 species, including the two new species described here, only A. cumulatus, A. leucocarpus, A. osmophilus and A. xerophilus have unique ITS barcodes. The alignments for the BenA, CaM and RPB2 datasets were respectively 389 (151 variable, 136 parsimony informative), 556 (221 variable, 177 parsimony informative) and 871 bp (202 variable, 162 parsimony informative) long. MP analy-ses resulted in 84 (length 287 steps, CI = 0.728, RI = 0.923), 12 (length 275 steps, CI = 0.7, RI = 0.904), 28 (length 364 steps, CI = 0.648, RI = 0.911) and 24 (length 798 steps, CI = 0.692, RI = 0.907) equally parsimonious trees for BenA, CaM, RPB2 and concatenated dataset. K80+G (BenA), SYM+G (CaM) and SYM+I+G (RPB2) were the most suitable models for BI.
Tree topologies did not differ for respective genes between MP and BI; therefore, MP trees were used to present results. Some species are consistently resolved as sister
A survey of xerophilic Aspergillus from indoor environment... 7
Tabl
e 1.
Str
ains
use
d fo
r phy
loge
netic
ana
lyse
s.
Gen
Ban
k ac
cess
ion
num
bers
Spec
ies
Stra
ins
Ori
gin
ITS
CaM
Ben
AR
PB2
Aspe
rgill
us a
ppen
dicu
latu
sC
BS 3
74.7
5T; D
AOM
C 2
3166
5; IM
I 278
374;
ET
H 8
286
Smok
ed sa
usag
e, Sw
itser
land
HE6
1513
2H
E801
318
HE8
0133
3H
E801
307
Aspe
rgill
us a
ppen
dicu
latu
sC
BS10
1746
; AS
3.46
73Sh
eep
dung
, Chi
naH
E615
133
HE8
0131
9H
E801
334
HE8
0130
8
Aspe
rgill
us b
runn
eus
CBS
112
.26T
; NRR
L131
; ATC
C 1
021;
IMI 2
1137
8; M
UC
L 15
646
Fig,
USA
EF65
2060
EF65
1998
EF65
1907
EF65
1939
Aspe
rgill
us b
runn
eus
CBS
113
.27;
NRR
L124
; ATC
C 1
036;
IMI 0
2918
8U
nkno
wn
EF65
2056
EF65
1997
EF65
1904
EF65
1938
Aspe
rgill
us b
runn
eus
NRR
L 13
3U
nkno
wn
EF65
2061
EF65
1999
EF65
1908
EF65
1940
Aspe
rgill
us ch
eval
ieri
CBS
522
.65T
; NRR
L 78
; ATC
C 1
6443
; IM
I 211
382
Coff
ee b
eans
, USA
EF65
2068
EF65
2002
EF65
1911
EF65
1954
Aspe
rgill
us ch
eval
ieri
NRR
L 47
55C
onta
min
ated
cultu
re, U
SAEF
6520
71EF
6520
04EF
6519
13EF
6519
56As
perg
illus
chev
alier
iN
RRL
79U
nkno
wn,
USA
EF65
2069
EF65
2003
EF65
1912
EF65
1955
Aspe
rgill
us ci
bariu
sK
ACC
463
46T
Meju
, Kor
eaJQ
9181
77JQ
9181
83JQ
9181
80JQ
9181
86As
perg
illus
ciba
rius
KAC
C 4
6764
Meju
, Kor
eaJQ
9181
78JQ
9181
84JQ
9181
81JQ
9181
87As
perg
illus
ciba
rius
KAC
C 4
6765
Meju
, Kor
eaJQ
9181
79JQ
9181
85JQ
9181
82JQ
9181
88As
perg
illus
costi
form
isC
BS 1
0174
9T; A
S 3.
4664
Rotte
n pa
per,
Chi
naH
E615
136
HE8
0132
0H
E801
338
HE8
0130
9
Aspe
rgill
us cr
istat
usC
BS 1
23.5
3T; N
RRL
4222
; ATC
C 1
6468
; IM
I 172
280;
M
UC
L 15
644
Unk
now
n, S
outh
Afri
caEF
6520
78EF
6520
01EF
6519
14EF
6519
57
Aspe
rgill
us cu
mul
atus
KAC
C 4
7316
TRi
ce st
raw,
Kor
eaK
F928
303
KF9
2830
0K
F928
297
KF9
2829
4
Aspe
rgill
us cu
mul
atus
KAC
C 4
7513
Indo
or ai
r fro
m m
eju fe
rmen
ta-
tion
room
, Kor
eaK
F928
304
KF9
2830
1K
F928
298
KF9
2829
5
Aspe
rgill
us cu
mul
atus
KAC
C 4
7514
Indo
or ai
r fro
m m
eju fe
rmen
ta-
tion
room
, Kor
eaK
F928
305
KF9
2830
2K
F928
299
KF9
2829
6
Aspe
rgill
us gl
aucu
sC
BS 5
16.6
5T; N
RRL
116;
ATC
C 1
6469
; IM
I 211
383
Unp
ainte
d ba
sem
ent b
oard
, USA
EF65
2052
EF65
1989
EF65
1887
EF65
1934
Aspe
rgill
us gl
aucu
sN
RRL
117;
ATC
C 6
6470
Unp
ainte
d ba
sem
ent b
oard
, USA
EF65
2053
EF65
1990
EF65
1888
EF65
1935
Aspe
rgill
us gl
aucu
sN
RRL
120;
ATC
C 1
6925
; FRR
120
Unk
now
nEF
6520
54EF
6519
91EF
6518
89EF
6519
36As
perg
illus
glau
cus
NRR
L 12
1; IM
I 313
756
Unk
now
nEF
6520
55EF
6519
92EF
6518
90EF
6519
37As
perg
illus
inter
med
ius
CBS
377
.75;
IMI 2
7837
6; E
TH
827
7So
il, S
pain
HE9
7445
9H
E974
437
HE9
7443
2H
E974
425
Aspe
rgill
us in
term
ediu
sC
BS 5
23.6
5T; N
RRL
82; A
TCC
164
44; I
MI 0
8927
8; IM
I 08
9278
ii; D
SM 2
830
Unk
now
n, U
nite
d K
ingd
omEF
6520
74EF
6520
12EF
6518
92EF
6519
58
Cobus M. Visagie et al. / MycoKeys 19: 1–30 (2017)8
Gen
Ban
k ac
cess
ion
num
bers
Spec
ies
Stra
ins
Ori
gin
ITS
CaM
Ben
AR
PB2
Aspe
rgill
us in
term
ediu
sN
RRL
4817
; IM
I 313
754
Unk
now
nEF
6520
72EF
6520
14EF
6518
94EF
6519
60As
perg
illus
inter
med
ius
NRR
L 84
Unk
now
nEF
6520
70EF
6520
13EF
6518
93EF
6519
59As
perg
illus
leuc
ocar
pus
CBS
353
.68T
; NRR
L349
7; IM
I 278
375
Raw
saus
age,
Ger
man
yEF
6520
87EF
6520
23EF
6519
25EF
6519
72As
perg
illus
mal
lochi
iD
AOM
C 1
4605
4T =
CBS
141
928
= D
TO 3
57A5
= K
AS 7
618
Pack
rat d
ung,
USA
KX4
5090
7K
X450
902
KX4
5088
9K
X450
894
Aspe
rgill
us m
alloc
hii
CBS
141
776
= D
TO 3
43G
3'C
hoco
lat m
iroir'
icin
g fo
r cak
e, th
e Net
herla
nds
KX4
5090
8K
X450
903
KX4
5089
0K
X450
895
Aspe
rgill
us m
egas
poru
sD
AOM
C 2
5079
9T =
CBS
141
929=
DTO
356
H7
= K
AS 6
176
Hou
se d
ust,
Can
ada
KX4
5091
0K
X450
905
KX4
5089
2K
X450
897
Aspe
rgill
us m
egas
poru
sD
AOM
C 2
5080
0 =
DTO
356
H1
= K
AS 5
973
Hou
se d
ust,
Can
ada
KX4
5090
9K
X450
904
KX4
5089
1K
X450
896
Aspe
rgill
us m
egas
poru
sC
BS 1
4177
2 =
DTO
048
I3D
utch
choc
olat
e but
ter,
the N
ethe
rland
sK
X450
911
KX4
5090
6K
X450
893
KX4
5089
8
Aspe
rgill
us m
ontev
iden
sisC
BS 4
91.6
5T; N
RRL
108;
ATC
C 1
0077
; IM
I 172
290;
IH
EM 3
337
Hum
an ty
mpa
nic m
embr
ane,
unkn
own
EF65
2077
EF65
2020
EF65
1898
EF65
1964
Aspe
rgill
us m
ontev
iden
sisC
BS 5
18.6
5; N
RRL9
0; A
TCC
164
64; I
MI 2
2997
1; IF
O 3
3018
Unk
now
n, U
SAEF
6520
76EF
6520
17EF
6518
97EF
6519
63As
perg
illus
mon
tevid
ensis
NRR
L 47
16; I
MI 3
5034
8C
andi
ed g
rape
fruit
rind,
USA
EF65
2079
EF65
2018
EF65
1899
EF65
1965
Aspe
rgill
us m
ontev
iden
sisN
RRL
89; A
TCC
100
65; I
MI 2
1180
6U
nkno
wn
EF65
2075
EF65
2016
EF65
1896
EF65
1962
Aspe
rgill
us n
eoca
rnoy
iC
BS 4
71.6
5T; N
RRL1
26; A
TCC
169
24; I
MI 1
7227
9U
nkno
wn
EF65
2057
EF65
1985
EF65
1903
EF65
1942
Aspe
rgill
us n
iveo
glauc
usC
BS 1
0175
0; A
S 3.
4665
Soil,
Chi
naH
E615
135
HE8
0132
3H
E801
331
HE8
0131
2
Aspe
rgill
us n
iveo
glauc
usC
BS 1
14.2
7T; N
RRL1
27; N
RRL
129;
NRR
L 13
0; A
TCC
10
075;
CBS
517
.65;
IMI 0
3205
0; IM
I 032
050i
iU
nkno
wn
EF65
2058
EF65
1993
EF65
1905
EF65
1943
Aspe
rgill
us n
iveo
glauc
usN
RRL
128;
FRR
128
; IM
I 091
871
Unk
now
nEF
6520
59EF
6519
94EF
6519
06EF
6519
44As
perg
illus
niv
eogla
ucus
NRR
L 13
6U
nkno
wn
EF65
2062
EF65
1995
EF65
1909
EF65
1945
Aspe
rgill
us n
iveo
glauc
usN
RRL
137;
IMI 0
9187
2U
nkno
wn
EF65
2063
EF65
1996
EF65
1910
EF65
1946
Aspe
rgill
us os
mop
hilu
sC
BS 1
3425
8T; I
RAN
209
0CLe
af o
f Trit
icum
aest
ivu,
Iran
KC47
3921
KC47
3918
KC47
3924
KX5
1231
0
Aspe
rgill
us p
rolif
erans
CBS
121
.45T
; NRR
L 19
08; C
BS 5
28.6
5; A
TCC
169
22; I
MI
0161
05; I
MI 0
1610
5ii;
IMI 0
1610
5iii;
MU
CL
1562
5C
otto
n ya
rn, U
nite
d K
ingd
omEF
6520
64EF
6519
88EF
6518
91EF
6519
41
Aspe
rgill
us p
rolif
erans
NRR
L 11
4; A
TCC
100
76; I
MI 2
1180
8U
nkno
wn,
USA
EF65
2051
EF65
1987
EF65
1886
EF65
1933
Aspe
rgill
us p
rolif
erans
NRR
L 62
482;
CC
F 40
96Pa
lm sk
in, C
zech
Rep
ublic
FR84
8827
HE6
5090
8FR
7753
75H
E801
303
Aspe
rgill
us p
rolif
erans
NRR
L 62
494;
CC
F 41
46To
enail
, Cze
ch R
epub
licH
E578
067
HE6
5090
9H
E578
076
HE8
0130
4As
perg
illus
pro
lifera
nsN
RRL
6249
7; C
CF
4115
Toen
ail, C
zech
Rep
ublic
FR85
1850
HE5
7809
0FR
8518
55H
E578
107
A survey of xerophilic Aspergillus from indoor environment... 9
Gen
Ban
k ac
cess
ion
num
bers
Spec
ies
Stra
ins
Ori
gin
ITS
CaM
Ben
AR
PB2
Aspe
rgill
us p
rolif
erans
NRR
L 71
Leaf
hopp
ers,
USA
EF65
2047
EF65
1986
EF65
1885
EF65
1932
Aspe
rgill
us p
seudo
glauc
usC
BS 1
23.2
8T; N
RRL
40; A
TCC
100
66; I
MI 0
1612
2; IM
I 01
6122
ii; M
UC
L 15
624
Unk
now
nEF
6520
50EF
6520
07EF
6519
17EF
6519
52
Aspe
rgill
us p
seudo
glauc
usC
BS 3
79.7
5; IM
I 278
373;
ET
H 8
218;
DSM
137
0Le
af fr
om V
accin
ium
myr
tillu
s, Sw
itser
land
HE6
1513
1H
E801
322
HE8
0133
6H
E801
311
Aspe
rgill
us p
seudo
glauc
usC
BS 5
29.6
5; N
RRL1
3; N
RRL
24; A
TCC
929
4; IM
I 016
114;
IM
I 016
114i
i; M
UC
L 15
649
Prun
us d
omes
tica,
Fran
ceEF
6520
48EF
6520
05EF
6519
15EF
6519
50
Aspe
rgill
us p
seudo
glauc
usC
BS10
1747
; AS
3.46
74An
imal
dung
, Chi
naH
E615
130
HE8
0132
1H
E801
335
HE8
0131
0As
perg
illus
pseu
dogla
ucus
NRR
L 17
; ATC
C 1
0079
; UAM
H 6
580
Skin
from
wris
t, U
SAEF
6520
49EF
6520
06EF
6519
16EF
6519
51As
perg
illus
rube
rC
BS 1
0174
8; A
S 3.
4632
Soil,
Chi
naH
E615
134
HE8
0132
5H
E801
337
HE8
0131
5As
perg
illus
rube
rC
BS 4
64.6
5; N
RRL5
000;
ATC
C 1
6923
; IM
I 320
48C
offee
bea
ns, U
nite
d K
ingd
omEF
6520
80EF
6520
10EF
6519
22EF
6519
49As
perg
illus
rube
rC
BS 5
30.6
5T; N
RRL
52; A
TCC
164
41; I
MI 2
1138
0U
nkno
wn
EF65
2066
EF65
2009
EF65
1920
EF65
1947
Aspe
rgill
us ru
ber
NRR
L 76
; IM
I 918
68U
nkno
wn
EF65
2067
EF65
2011
EF65
1921
EF65
1948
Aspe
rgill
us sl
oani
iC
BS 1
3817
6; D
TO 2
44-I8
Hou
se d
ust,
Uni
ted
Kin
gdom
KJ7
7553
9K
J775
308
KJ7
7507
3K
X463
364
Aspe
rgill
us sl
oani
iC
BS 1
3817
7T; D
TO 2
45-A
1H
ouse
dus
t, U
nite
d K
ingd
omK
J775
540
KJ7
7530
9K
J775
074
KX4
6336
5As
perg
illus
sloa
nii
CBS
138
178;
DTO
245
-A8
Hou
se d
ust,
Uni
ted
Kin
gdom
KJ7
7554
2K
J775
313
KJ7
7507
6K
X450
900
Aspe
rgill
us sl
oani
iC
BS 1
3817
9; D
TO 2
45-A
9H
ouse
dus
t, U
nite
d K
ingd
omK
J775
543
KJ7
7531
4K
J775
077
KX4
5090
1As
perg
illus
sloa
nii
CBS
138
231;
DTO
245
-A6
Hou
se d
ust,
Uni
ted
Kin
gdom
KJ7
7554
1K
J775
311
KJ7
7507
5K
X450
899
Aspe
rgill
us to
noph
ilus
CBS
405
.65T
; NRR
L 51
24; A
TCC
145
67; A
TCC
164
40;
ATC
C 3
6504
; DSM
346
2; IF
O 6
529;
IMI 1
0829
9; IM
I 10
8299
iiBi
nocu
lar le
ns, J
apan
EF65
2081
EF65
2000
EF65
1919
EF65
1969
Aspe
rgill
us x
erop
hilu
sC
BS 9
38.7
3T; N
RRL6
131;
FRR
280
4; IM
I 278
377
Des
ert s
oil,
Egyp
tEF
6520
85EF
6519
83EF
6519
23EF
6519
70As
perg
illus
xer
ophi
lus
NRR
L 61
32D
eser
t soi
l, Eg
ypt
EF65
2086
EF65
1984
EF65
1924
EF65
1971
Cobus M. Visagie et al. / MycoKeys 19: 1–30 (2017)10
7.0
A. chevalieri NRRL79
A. appendiculatus CBS374.75T
A. ruber CBS530.65T
A. pseudoglaucus CBS101747
A. brunneus NRRL124
A. montevidensis CBS491.65T
A. cumulatus KACC47513
A. montevidensis NRRL90
A. proliferans NRRL71
A. pseudoglaucus NRRL13
A. niveoglaucus NRRL137
A. proliferans NRRL114
A. pseudoglaucus CBS379.75
A. osmophilus CBS134258TA. xerophilus NRRL6132
A. intermedius CBS377.75
A. proliferans NRRL62497
A. glaucus CBS516.65T
A. cristatus CBS123.53T
A. intermedius NRRL84
A. ruber NRRL5000
A. tonophilus CBS405.65T
A. sloanii CBS138176
A. pseudoglaucus CBS123.28T
A. proliferans NRRL62482
A. niveoglaucus CBS101750
A. mallochii CBS141776
A. sloanii CBS138231A. sloanii CBS138179
A. megasporus DAOMC250799T
A. mallochii DAOMC146054T
A. glaucus NRRL117
A. appendiculatus CBS101746
A. pseudoglaucus NRRL17
A. chevalieri NRRL4755
A. cibarius KACC46765
A. proliferans CBS121.45T
A. cibarius KACC46346T
A. sloanii CBS138177T
A. megasporus CBS141772
A. cibarius KACC46764
A. montevidensis NRRL4716A. montevidensis NRRL89
A. ruber NRRL76A. cumulatus KACC47316T
A. brunneus NRRL133
A. niveoglaucus NRRL136
A. glaucus NRRL121
A. megasporus DAOMC250800
A. ruber CBS101748
A. neocarnoyi NRRL126T
A. leucocarpus NRRL3497T
A. costiformis CBS101749T
A. xerophilus NRRL6131T*/99
*/99
*/96
*/99
0.98/-
0.98/-
A. proliferans NRRL62494
A. sloanii CBS138178
A. intermedius CBS523.65T
A. chevalieri CBS522.65TITS
A. intermedius NRRL4817
A. niveoglaucus NRRL128
A. brunneus NRRL131T
A. glaucus NRRL120
A. niveoglaucus NRRL127T
A. cumulatus KACC47514
x2
*/99*/99
*/99
*/99
0.99/90
0.98/*
-/83
-/86
*/*
*/99
*/-
*/96
*/98
*/94
*/84
*/87
0.99/-
0.98/87
*/99
-/*
*/*
*/*
*/98
-/88
0.95/-
0.95/-
*/*
0.96/-
*/*
*/*
*/*
*/*
*/*
0.95/-
0.99/-
0.98/-
0.99/83*/95
*/84
*/*
*/*
*/99
*/*
*/*
*/*
*/94
0.97/97
*/*
BenA
x4
x4
x4
x4
x4
20.0
A. montevidensis NRRL90
A. niveoglaucus NRRL137
A. appendiculatus CBS374.75T
A. proliferans NRRL71
A. sloanii CBS138178
A. montevidensis NRRL4716
A. glaucus NRRL121
A. pseudoglaucus CBS123.28T
A. chevalieri NRRL79
A. appendiculatus CBS101746
A. cibarius KACC46765
A. neocarnoyi NRRL126T
A. cristatus CBS123.53T
A. tonophilus CBS405.65T
A. niveoglaucus NRRL127T
A. costiformis CBS101749T
A. sloanii CBS138177T
A. osmophilus CBS134258T
A. cumulatus KACC47513
A. sloanii CBS138231
A. proliferans CBS121.45T
A. mallochii DAOMC146054T
A. cumulatus KACC47316T
A. glaucus NRRL120
A. niveoglaucus NRRL136
A. brunneus NRRL124
A. brunneus NRRL133
A. proliferans NRRL62482
A. megasporus CBS141772
A. pseudoglaucus NRRL13
A. proliferans NRRL62497
A. sloanii CBS138179
A. intermedius CBS377.75
A. glaucus CBS516.65T
A. proliferans NRRL62494
A. brunneus NRRL131T
A. pseudoglaucus CBS101747
A. ruber NRRL5000
A. proliferans NRRL114
A. pseudoglaucus NRRL17
A. xerophilus NRRL6131T
A. sloanii CBS138176
A. glaucus NRRL117
A. leucocarpus NRRL3497T
A. niveoglaucus CBS101750
A. xerophilus NRRL6132
A. cibarius KACC46764
A. chevalieri NRRL4755
A. montevidensis NRRL89
A. ruber NRRL76
A. niveoglaucus NRRL128
A. cumulatus KACC47514
A. ruber CBS530.65T
A. megasporus DAOMC250799T
A. megasporus DAOMC250800
A. intermedius NRRL84A. montevidensis CBS491.65T
A. mallochii CBS141776
A. intermedius NRRL4817
A. ruber CBS101748
A. pseudoglaucus CBS379.75
A. intermedius CBS523.65T
A. chevalieri CBS522.65T
A. cibarius KACC46346T
*/**/*
*/**/*
*/*
*/*
*/99
*/87
*/91
*/97
*/96
*/*
*/84
*/*
*/*
*/*
*/*
*/*
*/**/*
*/*
*/94*/*
*/83
*/98
*/98
*/94
x4
x4
x4
x4
x4
x2
x2
CaM
20.0
A. intermedius NRRL84
A. brunneus NRRL131T
A. glaucus NRRL117
A. ruber CBS530.65T
A. glaucus CBS516.65T
A. intermedius CBS377.75
A. proliferans NRRL71
A. intermedius CBS523.65T
A. intermedius NRRL4817
A. pseudoglaucus NRRL17
A. tonophilus CBS405.65T
A. niveoglaucus CBS101750
A. pseudoglaucus CBS101747
A. glaucus NRRL121A. glaucus NRRL120
A. cumulatus KACC47316T
A. montevidensis NRRL4716
A. proliferans NRRL62497
A. appendiculatus CBS374.75T
A. cibarius KACC46346T
A. proliferans NRRL114
A. megasporus DAOMC250799T
A. megasporus CBS141772A. megasporus DAOMC250800
A. niveoglaucus NRRL127T
A. xerophilus NRRL6132
A. proliferans NRRL62482
A. mallochii CBS141776
A. montevidensis NRRL89
A. sloanii CBS138177T
A. chevalieri NRRL79
A. proliferans CBS121.45T
A. proliferans NRRL62494
A. ruber NRRL5000
A. chevalieri NRRL4755
A. niveoglaucus NRRL136A. niveoglaucus NRRL128
A. appendiculatus CBS101746
A. ruber NRRL76
A. cibarius KACC46765
A. cristatus CBS123.53T
A. sloanii CBS138179
A. pseudoglaucus NRRL13
A. leucocarpus NRRL3497T
A. cibarius KACC46764
A. sloanii CBS138176
A. cumulatus KACC47513
A. montevidensis NRRL90
A. niveoglaucus NRRL137
A. ruber CBS101748
A. sloanii CBS138178
A. mallochii DAOMC146054T
A. pseudoglaucus CBS379.75A. pseudoglaucus CBS123.28T
A. cumulatus KACC47514
A. montevidensis CBS491.65T
A. xerophilus NRRL6131T
A. costiformis CBS101749T
A. neocarnoyi NRRL126T
A. chevalieri CBS522.65T
A. sloanii CBS138231
A. brunneus NRRL133A. brunneus NRRL124
A. osmophilus CBS134258T
RPB2
x4
x4
x4
20.0
A. niveoglaucus NRRL127T
A. mallochii CBS141776
A. glaucus CBS516.65T
A. pseudoglaucus NRRL13
A. sloanii CBS138179
A. montevidensis NRRL89
A. sloanii CBS138177T
A. pseudoglaucus CBS379.75
A. cibarius KACC46764
A. niveoglaucus NRRL137
A. niveoglaucus NRRL128
A. sloanii CBS138178
A. brunneus NRRL124
A. cibarius KACC46346T
A. cristatus CBS123.53T
A. pseudoglaucus CBS123.28T
A. chevalieri NRRL4755
A. osmophilus CBS134258T
A. megasporus CBS141772
A. ruber NRRL76
A. montevidensis CBS491.65T
A. neocarnoyi NRRL126T
A. mallochii DAOMC146054T
A. intermedius NRRL84
A. ruber NRRL5000
A. brunneus NRRL133
A. niveoglaucus NRRL136
A. cumulatus KACC47513
A. proliferans NRRL62494
A. niveoglaucus CBS101750
A. intermedius NRRL4817
A. proliferans NRRL62497
A. intermedius CBS523.65T
A. xerophilus NRRL6131T
A. chevalieri CBS522.65T
A. cumulatus KACC47316T
A. proliferans NRRL114
A. cumulatus KACC47514
A. xerophilus NRRL6132
A. brunneus NRRL131T
A. montevidensis NRRL90
A. glaucus NRRL117
A. pseudoglaucus NRRL17
A. leucocarpus NRRL3497T
A. proliferans NRRL62482
A. montevidensis NRRL4716
A. tonophilus CBS405.65T
A. sloanii CBS138176
A. megasporus DAOMC250799T
A. costiformis CBS101749T
A. cibarius KACC46765
A. proliferans NRRL71
A. appendiculatus CBS101746
A. intermedius CBS377.75
A. ruber CBS530.65T
A. pseudoglaucus CBS101747
A. sloanii CBS138231
A. glaucus NRRL121
A. chevalieri NRRL79
A. glaucus NRRL120
A. appendiculatus CBS374.75T
A. ruber CBS101748
A. proliferans CBS121.45T
A. megasporus DAOMC250800
Figure 1. One of the most parsimonious trees of Aspergillus sect. Aspergillus based on ITS, CaM, BenA and RPB2. Trees were rooted to A. xerophilus, A. leucocarpus and A. osmophilus. Support in nodes higher than 80% bootstrap values and 0.95 posterior probabilities are shown above thickened branches. New species are shown in bold and colour, while ex-type strains are followed by T.
A survey of xerophilic Aspergillus from indoor environment... 11
7.0
A. chevalieri NRRL79
A. appendiculatus CBS374.75T
A. ruber CBS530.65T
A. pseudoglaucus CBS101747
A. brunneus NRRL124
A. montevidensis CBS491.65T
A. cumulatus KACC47513
A. montevidensis NRRL90
A. proliferans NRRL71
A. pseudoglaucus NRRL13
A. niveoglaucus NRRL137
A. proliferans NRRL114
A. pseudoglaucus CBS379.75
A. osmophilus CBS134258TA. xerophilus NRRL6132
A. intermedius CBS377.75
A. proliferans NRRL62497
A. glaucus CBS516.65T
A. cristatus CBS123.53T
A. intermedius NRRL84
A. ruber NRRL5000
A. tonophilus CBS405.65T
A. sloanii CBS138176
A. pseudoglaucus CBS123.28T
A. proliferans NRRL62482
A. niveoglaucus CBS101750
A. mallochii CBS141776
A. sloanii CBS138231A. sloanii CBS138179
A. megasporus DAOMC250799T
A. mallochii DAOMC146054T
A. glaucus NRRL117
A. appendiculatus CBS101746
A. pseudoglaucus NRRL17
A. chevalieri NRRL4755
A. cibarius KACC46765
A. proliferans CBS121.45T
A. cibarius KACC46346T
A. sloanii CBS138177T
A. megasporus CBS141772
A. cibarius KACC46764
A. montevidensis NRRL4716A. montevidensis NRRL89
A. ruber NRRL76A. cumulatus KACC47316T
A. brunneus NRRL133
A. niveoglaucus NRRL136
A. glaucus NRRL121
A. megasporus DAOMC250800
A. ruber CBS101748
A. neocarnoyi NRRL126T
A. leucocarpus NRRL3497T
A. costiformis CBS101749T
A. xerophilus NRRL6131T*/99
*/99
*/96
*/99
0.98/-
0.98/-
A. proliferans NRRL62494
A. sloanii CBS138178
A. intermedius CBS523.65T
A. chevalieri CBS522.65TITS
A. intermedius NRRL4817
A. niveoglaucus NRRL128
A. brunneus NRRL131T
A. glaucus NRRL120
A. niveoglaucus NRRL127T
A. cumulatus KACC47514
x2
*/99*/99
*/99
*/99
0.99/90
0.98/*
-/83
-/86
*/*
*/99
*/-
*/96
*/98
*/94
*/84
*/87
0.99/-
0.98/87
*/99
-/*
*/*
*/*
*/98
-/88
0.95/-
0.95/-
*/*
0.96/-
*/*
*/*
*/*
*/*
*/*
0.95/-
0.99/-
0.98/-
0.99/83*/95
*/84
*/*
*/*
*/99
*/*
*/*
*/*
*/94
0.97/97
*/*
BenA
x4
x4
x4
x4
x4
20.0
A. montevidensis NRRL90
A. niveoglaucus NRRL137
A. appendiculatus CBS374.75T
A. proliferans NRRL71
A. sloanii CBS138178
A. montevidensis NRRL4716
A. glaucus NRRL121
A. pseudoglaucus CBS123.28T
A. chevalieri NRRL79
A. appendiculatus CBS101746
A. cibarius KACC46765
A. neocarnoyi NRRL126T
A. cristatus CBS123.53T
A. tonophilus CBS405.65T
A. niveoglaucus NRRL127T
A. costiformis CBS101749T
A. sloanii CBS138177T
A. osmophilus CBS134258T
A. cumulatus KACC47513
A. sloanii CBS138231
A. proliferans CBS121.45T
A. mallochii DAOMC146054T
A. cumulatus KACC47316T
A. glaucus NRRL120
A. niveoglaucus NRRL136
A. brunneus NRRL124
A. brunneus NRRL133
A. proliferans NRRL62482
A. megasporus CBS141772
A. pseudoglaucus NRRL13
A. proliferans NRRL62497
A. sloanii CBS138179
A. intermedius CBS377.75
A. glaucus CBS516.65T
A. proliferans NRRL62494
A. brunneus NRRL131T
A. pseudoglaucus CBS101747
A. ruber NRRL5000
A. proliferans NRRL114
A. pseudoglaucus NRRL17
A. xerophilus NRRL6131T
A. sloanii CBS138176
A. glaucus NRRL117
A. leucocarpus NRRL3497T
A. niveoglaucus CBS101750
A. xerophilus NRRL6132
A. cibarius KACC46764
A. chevalieri NRRL4755
A. montevidensis NRRL89
A. ruber NRRL76
A. niveoglaucus NRRL128
A. cumulatus KACC47514
A. ruber CBS530.65T
A. megasporus DAOMC250799T
A. megasporus DAOMC250800
A. intermedius NRRL84A. montevidensis CBS491.65T
A. mallochii CBS141776
A. intermedius NRRL4817
A. ruber CBS101748
A. pseudoglaucus CBS379.75
A. intermedius CBS523.65T
A. chevalieri CBS522.65T
A. cibarius KACC46346T
*/**/*
*/**/*
*/*
*/*
*/99
*/87
*/91
*/97
*/96
*/*
*/84
*/*
*/*
*/*
*/*
*/*
*/**/*
*/*
*/94*/*
*/83
*/98
*/98
*/94
x4
x4
x4
x4
x4
x2
x2
CaM
20.0
A. intermedius NRRL84
A. brunneus NRRL131T
A. glaucus NRRL117
A. ruber CBS530.65T
A. glaucus CBS516.65T
A. intermedius CBS377.75
A. proliferans NRRL71
A. intermedius CBS523.65T
A. intermedius NRRL4817
A. pseudoglaucus NRRL17
A. tonophilus CBS405.65T
A. niveoglaucus CBS101750
A. pseudoglaucus CBS101747
A. glaucus NRRL121A. glaucus NRRL120
A. cumulatus KACC47316T
A. montevidensis NRRL4716
A. proliferans NRRL62497
A. appendiculatus CBS374.75T
A. cibarius KACC46346T
A. proliferans NRRL114
A. megasporus DAOMC250799T
A. megasporus CBS141772A. megasporus DAOMC250800
A. niveoglaucus NRRL127T
A. xerophilus NRRL6132
A. proliferans NRRL62482
A. mallochii CBS141776
A. montevidensis NRRL89
A. sloanii CBS138177T
A. chevalieri NRRL79
A. proliferans CBS121.45T
A. proliferans NRRL62494
A. ruber NRRL5000
A. chevalieri NRRL4755
A. niveoglaucus NRRL136A. niveoglaucus NRRL128
A. appendiculatus CBS101746
A. ruber NRRL76
A. cibarius KACC46765
A. cristatus CBS123.53T
A. sloanii CBS138179
A. pseudoglaucus NRRL13
A. leucocarpus NRRL3497T
A. cibarius KACC46764
A. sloanii CBS138176
A. cumulatus KACC47513
A. montevidensis NRRL90
A. niveoglaucus NRRL137
A. ruber CBS101748
A. sloanii CBS138178
A. mallochii DAOMC146054T
A. pseudoglaucus CBS379.75A. pseudoglaucus CBS123.28T
A. cumulatus KACC47514
A. montevidensis CBS491.65T
A. xerophilus NRRL6131T
A. costiformis CBS101749T
A. neocarnoyi NRRL126T
A. chevalieri CBS522.65T
A. sloanii CBS138231
A. brunneus NRRL133A. brunneus NRRL124
A. osmophilus CBS134258T
RPB2
x4
x4
x4
20.0
A. niveoglaucus NRRL127T
A. mallochii CBS141776
A. glaucus CBS516.65T
A. pseudoglaucus NRRL13
A. sloanii CBS138179
A. montevidensis NRRL89
A. sloanii CBS138177T
A. pseudoglaucus CBS379.75
A. cibarius KACC46764
A. niveoglaucus NRRL137
A. niveoglaucus NRRL128
A. sloanii CBS138178
A. brunneus NRRL124
A. cibarius KACC46346T
A. cristatus CBS123.53T
A. pseudoglaucus CBS123.28T
A. chevalieri NRRL4755
A. osmophilus CBS134258T
A. megasporus CBS141772
A. ruber NRRL76
A. montevidensis CBS491.65T
A. neocarnoyi NRRL126T
A. mallochii DAOMC146054T
A. intermedius NRRL84
A. ruber NRRL5000
A. brunneus NRRL133
A. niveoglaucus NRRL136
A. cumulatus KACC47513
A. proliferans NRRL62494
A. niveoglaucus CBS101750
A. intermedius NRRL4817
A. proliferans NRRL62497
A. intermedius CBS523.65T
A. xerophilus NRRL6131T
A. chevalieri CBS522.65T
A. cumulatus KACC47316T
A. proliferans NRRL114
A. cumulatus KACC47514
A. xerophilus NRRL6132
A. brunneus NRRL131T
A. montevidensis NRRL90
A. glaucus NRRL117
A. pseudoglaucus NRRL17
A. leucocarpus NRRL3497T
A. proliferans NRRL62482
A. montevidensis NRRL4716
A. tonophilus CBS405.65T
A. sloanii CBS138176
A. megasporus DAOMC250799T
A. costiformis CBS101749T
A. cibarius KACC46765
A. proliferans NRRL71
A. appendiculatus CBS101746
A. intermedius CBS377.75
A. ruber CBS530.65T
A. pseudoglaucus CBS101747
A. sloanii CBS138231
A. glaucus NRRL121
A. chevalieri NRRL79
A. glaucus NRRL120
A. appendiculatus CBS374.75T
A. ruber CBS101748
A. proliferans CBS121.45T
A. megasporus DAOMC250800
Figure 1. Continued.
Cobus M. Visagie et al. / MycoKeys 19: 1–30 (2017)12
7.0
A. chevalieri NRRL79
A. appendiculatus CBS374.75T
A. ruber CBS530.65T
A. pseudoglaucus CBS101747
A. brunneus NRRL124
A. montevidensis CBS491.65T
A. cumulatus KACC47513
A. montevidensis NRRL90
A. proliferans NRRL71
A. pseudoglaucus NRRL13
A. niveoglaucus NRRL137
A. proliferans NRRL114
A. pseudoglaucus CBS379.75
A. osmophilus CBS134258TA. xerophilus NRRL6132
A. intermedius CBS377.75
A. proliferans NRRL62497
A. glaucus CBS516.65T
A. cristatus CBS123.53T
A. intermedius NRRL84
A. ruber NRRL5000
A. tonophilus CBS405.65T
A. sloanii CBS138176
A. pseudoglaucus CBS123.28T
A. proliferans NRRL62482
A. niveoglaucus CBS101750
A. mallochii CBS141776
A. sloanii CBS138231A. sloanii CBS138179
A. megasporus DAOMC250799T
A. mallochii DAOMC146054T
A. glaucus NRRL117
A. appendiculatus CBS101746
A. pseudoglaucus NRRL17
A. chevalieri NRRL4755
A. cibarius KACC46765
A. proliferans CBS121.45T
A. cibarius KACC46346T
A. sloanii CBS138177T
A. megasporus CBS141772
A. cibarius KACC46764
A. montevidensis NRRL4716A. montevidensis NRRL89
A. ruber NRRL76A. cumulatus KACC47316T
A. brunneus NRRL133
A. niveoglaucus NRRL136
A. glaucus NRRL121
A. megasporus DAOMC250800
A. ruber CBS101748
A. neocarnoyi NRRL126T
A. leucocarpus NRRL3497T
A. costiformis CBS101749T
A. xerophilus NRRL6131T*/99
*/99
*/96
*/99
0.98/-
0.98/-
A. proliferans NRRL62494
A. sloanii CBS138178
A. intermedius CBS523.65T
A. chevalieri CBS522.65TITS
A. intermedius NRRL4817
A. niveoglaucus NRRL128
A. brunneus NRRL131T
A. glaucus NRRL120
A. niveoglaucus NRRL127T
A. cumulatus KACC47514
x2
*/99*/99
*/99
*/99
0.99/90
0.98/*
-/83
-/86
*/*
*/99
*/-
*/96
*/98
*/94
*/84
*/87
0.99/-
0.98/87
*/99
-/*
*/*
*/*
*/98
-/88
0.95/-
0.95/-
*/*
0.96/-
*/*
*/*
*/*
*/*
*/*
0.95/-
0.99/-
0.98/-
0.99/83*/95
*/84
*/*
*/*
*/99
*/*
*/*
*/*
*/94
0.97/97
*/*
BenA
x4
x4
x4
x4
x4
20.0
A. montevidensis NRRL90
A. niveoglaucus NRRL137
A. appendiculatus CBS374.75T
A. proliferans NRRL71
A. sloanii CBS138178
A. montevidensis NRRL4716
A. glaucus NRRL121
A. pseudoglaucus CBS123.28T
A. chevalieri NRRL79
A. appendiculatus CBS101746
A. cibarius KACC46765
A. neocarnoyi NRRL126T
A. cristatus CBS123.53T
A. tonophilus CBS405.65T
A. niveoglaucus NRRL127T
A. costiformis CBS101749T
A. sloanii CBS138177T
A. osmophilus CBS134258T
A. cumulatus KACC47513
A. sloanii CBS138231
A. proliferans CBS121.45T
A. mallochii DAOMC146054T
A. cumulatus KACC47316T
A. glaucus NRRL120
A. niveoglaucus NRRL136
A. brunneus NRRL124
A. brunneus NRRL133
A. proliferans NRRL62482
A. megasporus CBS141772
A. pseudoglaucus NRRL13
A. proliferans NRRL62497
A. sloanii CBS138179
A. intermedius CBS377.75
A. glaucus CBS516.65T
A. proliferans NRRL62494
A. brunneus NRRL131T
A. pseudoglaucus CBS101747
A. ruber NRRL5000
A. proliferans NRRL114
A. pseudoglaucus NRRL17
A. xerophilus NRRL6131T
A. sloanii CBS138176
A. glaucus NRRL117
A. leucocarpus NRRL3497T
A. niveoglaucus CBS101750
A. xerophilus NRRL6132
A. cibarius KACC46764
A. chevalieri NRRL4755
A. montevidensis NRRL89
A. ruber NRRL76
A. niveoglaucus NRRL128
A. cumulatus KACC47514
A. ruber CBS530.65T
A. megasporus DAOMC250799T
A. megasporus DAOMC250800
A. intermedius NRRL84A. montevidensis CBS491.65T
A. mallochii CBS141776
A. intermedius NRRL4817
A. ruber CBS101748
A. pseudoglaucus CBS379.75
A. intermedius CBS523.65T
A. chevalieri CBS522.65T
A. cibarius KACC46346T
*/**/*
*/**/*
*/*
*/*
*/99
*/87
*/91
*/97
*/96
*/*
*/84
*/*
*/*
*/*
*/*
*/*
*/**/*
*/*
*/94*/*
*/83
*/98
*/98
*/94
x4
x4
x4
x4
x4
x2
x2
CaM
20.0
A. intermedius NRRL84
A. brunneus NRRL131T
A. glaucus NRRL117
A. ruber CBS530.65T
A. glaucus CBS516.65T
A. intermedius CBS377.75
A. proliferans NRRL71
A. intermedius CBS523.65T
A. intermedius NRRL4817
A. pseudoglaucus NRRL17
A. tonophilus CBS405.65T
A. niveoglaucus CBS101750
A. pseudoglaucus CBS101747
A. glaucus NRRL121A. glaucus NRRL120
A. cumulatus KACC47316T
A. montevidensis NRRL4716
A. proliferans NRRL62497
A. appendiculatus CBS374.75T
A. cibarius KACC46346T
A. proliferans NRRL114
A. megasporus DAOMC250799T
A. megasporus CBS141772A. megasporus DAOMC250800
A. niveoglaucus NRRL127T
A. xerophilus NRRL6132
A. proliferans NRRL62482
A. mallochii CBS141776
A. montevidensis NRRL89
A. sloanii CBS138177T
A. chevalieri NRRL79
A. proliferans CBS121.45T
A. proliferans NRRL62494
A. ruber NRRL5000
A. chevalieri NRRL4755
A. niveoglaucus NRRL136A. niveoglaucus NRRL128
A. appendiculatus CBS101746
A. ruber NRRL76
A. cibarius KACC46765
A. cristatus CBS123.53T
A. sloanii CBS138179
A. pseudoglaucus NRRL13
A. leucocarpus NRRL3497T
A. cibarius KACC46764
A. sloanii CBS138176
A. cumulatus KACC47513
A. montevidensis NRRL90
A. niveoglaucus NRRL137
A. ruber CBS101748
A. sloanii CBS138178
A. mallochii DAOMC146054T
A. pseudoglaucus CBS379.75A. pseudoglaucus CBS123.28T
A. cumulatus KACC47514
A. montevidensis CBS491.65T
A. xerophilus NRRL6131T
A. costiformis CBS101749T
A. neocarnoyi NRRL126T
A. chevalieri CBS522.65T
A. sloanii CBS138231
A. brunneus NRRL133A. brunneus NRRL124
A. osmophilus CBS134258T
RPB2
x4
x4
x4
20.0
A. niveoglaucus NRRL127T
A. mallochii CBS141776
A. glaucus CBS516.65T
A. pseudoglaucus NRRL13
A. sloanii CBS138179
A. montevidensis NRRL89
A. sloanii CBS138177T
A. pseudoglaucus CBS379.75
A. cibarius KACC46764
A. niveoglaucus NRRL137
A. niveoglaucus NRRL128
A. sloanii CBS138178
A. brunneus NRRL124
A. cibarius KACC46346T
A. cristatus CBS123.53T
A. pseudoglaucus CBS123.28T
A. chevalieri NRRL4755
A. osmophilus CBS134258T
A. megasporus CBS141772
A. ruber NRRL76
A. montevidensis CBS491.65T
A. neocarnoyi NRRL126T
A. mallochii DAOMC146054T
A. intermedius NRRL84
A. ruber NRRL5000
A. brunneus NRRL133
A. niveoglaucus NRRL136
A. cumulatus KACC47513
A. proliferans NRRL62494
A. niveoglaucus CBS101750
A. intermedius NRRL4817
A. proliferans NRRL62497
A. intermedius CBS523.65T
A. xerophilus NRRL6131T
A. chevalieri CBS522.65T
A. cumulatus KACC47316T
A. proliferans NRRL114
A. cumulatus KACC47514
A. xerophilus NRRL6132
A. brunneus NRRL131T
A. montevidensis NRRL90
A. glaucus NRRL117
A. pseudoglaucus NRRL17
A. leucocarpus NRRL3497T
A. proliferans NRRL62482
A. montevidensis NRRL4716
A. tonophilus CBS405.65T
A. sloanii CBS138176
A. megasporus DAOMC250799T
A. costiformis CBS101749T
A. cibarius KACC46765
A. proliferans NRRL71
A. appendiculatus CBS101746
A. intermedius CBS377.75
A. ruber CBS530.65T
A. pseudoglaucus CBS101747
A. sloanii CBS138231
A. glaucus NRRL121
A. chevalieri NRRL79
A. glaucus NRRL120
A. appendiculatus CBS374.75T
A. ruber CBS101748
A. proliferans CBS121.45T
A. megasporus DAOMC250800
Figure 1. Continued.
A survey of xerophilic Aspergillus from indoor environment... 13
7.0
A. chevalieri NRRL79
A. appendiculatus CBS374.75T
A. ruber CBS530.65T
A. pseudoglaucus CBS101747
A. brunneus NRRL124
A. montevidensis CBS491.65T
A. cumulatus KACC47513
A. montevidensis NRRL90
A. proliferans NRRL71
A. pseudoglaucus NRRL13
A. niveoglaucus NRRL137
A. proliferans NRRL114
A. pseudoglaucus CBS379.75
A. osmophilus CBS134258TA. xerophilus NRRL6132
A. intermedius CBS377.75
A. proliferans NRRL62497
A. glaucus CBS516.65T
A. cristatus CBS123.53T
A. intermedius NRRL84
A. ruber NRRL5000
A. tonophilus CBS405.65T
A. sloanii CBS138176
A. pseudoglaucus CBS123.28T
A. proliferans NRRL62482
A. niveoglaucus CBS101750
A. mallochii CBS141776
A. sloanii CBS138231A. sloanii CBS138179
A. megasporus DAOMC250799T
A. mallochii DAOMC146054T
A. glaucus NRRL117
A. appendiculatus CBS101746
A. pseudoglaucus NRRL17
A. chevalieri NRRL4755
A. cibarius KACC46765
A. proliferans CBS121.45T
A. cibarius KACC46346T
A. sloanii CBS138177T
A. megasporus CBS141772
A. cibarius KACC46764
A. montevidensis NRRL4716A. montevidensis NRRL89
A. ruber NRRL76A. cumulatus KACC47316T
A. brunneus NRRL133
A. niveoglaucus NRRL136
A. glaucus NRRL121
A. megasporus DAOMC250800
A. ruber CBS101748
A. neocarnoyi NRRL126T
A. leucocarpus NRRL3497T
A. costiformis CBS101749T
A. xerophilus NRRL6131T*/99
*/99
*/96
*/99
0.98/-
0.98/-
A. proliferans NRRL62494
A. sloanii CBS138178
A. intermedius CBS523.65T
A. chevalieri CBS522.65TITS
A. intermedius NRRL4817
A. niveoglaucus NRRL128
A. brunneus NRRL131T
A. glaucus NRRL120
A. niveoglaucus NRRL127T
A. cumulatus KACC47514
x2
*/99*/99
*/99
*/99
0.99/90
0.98/*
-/83
-/86
*/*
*/99
*/-
*/96
*/98
*/94
*/84
*/87
0.99/-
0.98/87
*/99
-/*
*/*
*/*
*/98
-/88
0.95/-
0.95/-
*/*
0.96/-
*/*
*/*
*/*
*/*
*/*
0.95/-
0.99/-
0.98/-
0.99/83*/95
*/84
*/*
*/*
*/99
*/*
*/*
*/*
*/94
0.97/97
*/*
BenA
x4
x4
x4
x4
x4
20.0
A. montevidensis NRRL90
A. niveoglaucus NRRL137
A. appendiculatus CBS374.75T
A. proliferans NRRL71
A. sloanii CBS138178
A. montevidensis NRRL4716
A. glaucus NRRL121
A. pseudoglaucus CBS123.28T
A. chevalieri NRRL79
A. appendiculatus CBS101746
A. cibarius KACC46765
A. neocarnoyi NRRL126T
A. cristatus CBS123.53T
A. tonophilus CBS405.65T
A. niveoglaucus NRRL127T
A. costiformis CBS101749T
A. sloanii CBS138177T
A. osmophilus CBS134258T
A. cumulatus KACC47513
A. sloanii CBS138231
A. proliferans CBS121.45T
A. mallochii DAOMC146054T
A. cumulatus KACC47316T
A. glaucus NRRL120
A. niveoglaucus NRRL136
A. brunneus NRRL124
A. brunneus NRRL133
A. proliferans NRRL62482
A. megasporus CBS141772
A. pseudoglaucus NRRL13
A. proliferans NRRL62497
A. sloanii CBS138179
A. intermedius CBS377.75
A. glaucus CBS516.65T
A. proliferans NRRL62494
A. brunneus NRRL131T
A. pseudoglaucus CBS101747
A. ruber NRRL5000
A. proliferans NRRL114
A. pseudoglaucus NRRL17
A. xerophilus NRRL6131T
A. sloanii CBS138176
A. glaucus NRRL117
A. leucocarpus NRRL3497T
A. niveoglaucus CBS101750
A. xerophilus NRRL6132
A. cibarius KACC46764
A. chevalieri NRRL4755
A. montevidensis NRRL89
A. ruber NRRL76
A. niveoglaucus NRRL128
A. cumulatus KACC47514
A. ruber CBS530.65T
A. megasporus DAOMC250799T
A. megasporus DAOMC250800
A. intermedius NRRL84A. montevidensis CBS491.65T
A. mallochii CBS141776
A. intermedius NRRL4817
A. ruber CBS101748
A. pseudoglaucus CBS379.75
A. intermedius CBS523.65T
A. chevalieri CBS522.65T
A. cibarius KACC46346T
*/**/*
*/**/*
*/*
*/*
*/99
*/87
*/91
*/97
*/96
*/*
*/84
*/*
*/*
*/*
*/*
*/*
*/**/*
*/*
*/94*/*
*/83
*/98
*/98
*/94
x4
x4
x4
x4
x4
x2
x2
CaM
20.0
A. intermedius NRRL84
A. brunneus NRRL131T
A. glaucus NRRL117
A. ruber CBS530.65T
A. glaucus CBS516.65T
A. intermedius CBS377.75
A. proliferans NRRL71
A. intermedius CBS523.65T
A. intermedius NRRL4817
A. pseudoglaucus NRRL17
A. tonophilus CBS405.65T
A. niveoglaucus CBS101750
A. pseudoglaucus CBS101747
A. glaucus NRRL121A. glaucus NRRL120
A. cumulatus KACC47316T
A. montevidensis NRRL4716
A. proliferans NRRL62497
A. appendiculatus CBS374.75T
A. cibarius KACC46346T
A. proliferans NRRL114
A. megasporus DAOMC250799T
A. megasporus CBS141772A. megasporus DAOMC250800
A. niveoglaucus NRRL127T
A. xerophilus NRRL6132
A. proliferans NRRL62482
A. mallochii CBS141776
A. montevidensis NRRL89
A. sloanii CBS138177T
A. chevalieri NRRL79
A. proliferans CBS121.45T
A. proliferans NRRL62494
A. ruber NRRL5000
A. chevalieri NRRL4755
A. niveoglaucus NRRL136A. niveoglaucus NRRL128
A. appendiculatus CBS101746
A. ruber NRRL76
A. cibarius KACC46765
A. cristatus CBS123.53T
A. sloanii CBS138179
A. pseudoglaucus NRRL13
A. leucocarpus NRRL3497T
A. cibarius KACC46764
A. sloanii CBS138176
A. cumulatus KACC47513
A. montevidensis NRRL90
A. niveoglaucus NRRL137
A. ruber CBS101748
A. sloanii CBS138178
A. mallochii DAOMC146054T
A. pseudoglaucus CBS379.75A. pseudoglaucus CBS123.28T
A. cumulatus KACC47514
A. montevidensis CBS491.65T
A. xerophilus NRRL6131T
A. costiformis CBS101749T
A. neocarnoyi NRRL126T
A. chevalieri CBS522.65T
A. sloanii CBS138231
A. brunneus NRRL133A. brunneus NRRL124
A. osmophilus CBS134258T
RPB2
x4
x4
x4
20.0
A. niveoglaucus NRRL127T
A. mallochii CBS141776
A. glaucus CBS516.65T
A. pseudoglaucus NRRL13
A. sloanii CBS138179
A. montevidensis NRRL89
A. sloanii CBS138177T
A. pseudoglaucus CBS379.75
A. cibarius KACC46764
A. niveoglaucus NRRL137
A. niveoglaucus NRRL128
A. sloanii CBS138178
A. brunneus NRRL124
A. cibarius KACC46346T
A. cristatus CBS123.53T
A. pseudoglaucus CBS123.28T
A. chevalieri NRRL4755
A. osmophilus CBS134258T
A. megasporus CBS141772
A. ruber NRRL76
A. montevidensis CBS491.65T
A. neocarnoyi NRRL126T
A. mallochii DAOMC146054T
A. intermedius NRRL84
A. ruber NRRL5000
A. brunneus NRRL133
A. niveoglaucus NRRL136
A. cumulatus KACC47513
A. proliferans NRRL62494
A. niveoglaucus CBS101750
A. intermedius NRRL4817
A. proliferans NRRL62497
A. intermedius CBS523.65T
A. xerophilus NRRL6131T
A. chevalieri CBS522.65T
A. cumulatus KACC47316T
A. proliferans NRRL114
A. cumulatus KACC47514
A. xerophilus NRRL6132
A. brunneus NRRL131T
A. montevidensis NRRL90
A. glaucus NRRL117
A. pseudoglaucus NRRL17
A. leucocarpus NRRL3497T
A. proliferans NRRL62482
A. montevidensis NRRL4716
A. tonophilus CBS405.65T
A. sloanii CBS138176
A. megasporus DAOMC250799T
A. costiformis CBS101749T
A. cibarius KACC46765
A. proliferans NRRL71
A. appendiculatus CBS101746
A. intermedius CBS377.75
A. ruber CBS530.65T
A. pseudoglaucus CBS101747
A. sloanii CBS138231
A. glaucus NRRL121
A. chevalieri NRRL79
A. glaucus NRRL120
A. appendiculatus CBS374.75T
A. ruber CBS101748
A. proliferans CBS121.45T
A. megasporus DAOMC250800
Figure 1. Continued.
Cobus M. Visagie et al. / MycoKeys 19: 1–30 (2017)14
*/**/*
*/*
*/*
*/*
*/99
*/90
*/99
*/98*/92
*/**/97
*/*
*/98 */**/87
*/99*/*
0.99/91
0.97/-
*/95
*/*
*/82
*/*
*/*
*/*0.97/81
0.97/-
*/*
*/*
*/**/*
*/*
*/*
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*/*
*/*
*/**/96
ConcatenatedITS + BenA + CaM + RPB2
x4
x2
x2
x4
50.0
A. mallochii DAOMC146054T
A. cumulatus KACC47513
A. leucocarpus NRRL3497T
A. niveoglaucus CBS101750
A. intermedius NRRL4817
A. montevidensis NRRL4716
A. proliferans NRRL62497
A. pseudoglaucus NRRL17
A. brunneus NRRL124
A. cibarius KACC46346T
A. pseudoglaucus CBS123.28T
A. proliferans NRRL62494
A. montevidensis NRRL89
A. sloanii CBS138177T
A. pseudoglaucus NRRL13
A. cumulatus KACC47316T
A. megasporus DAOMC250800
A. brunneus NRRL131T
A. tonophilus CBS405.65T
A. proliferans NRRL71
A. cibarius KACC46764
A. xerophilus NRRL6131T
A. ruber NRRL76
A. intermedius CBS523.65T
A. ruber NRRL5000
A. sloanii CBS138179
A. cumulatus KACC47514
A. sloanii CBS138176
A. intermedius NRRL84
A. appendiculatus CBS101746
A. megasporus CBS141772
A. chevalieri NRRL79
A. glaucus CBS516.65T
A. chevalieri CBS522.65T
A. mallochii CBS141776
A. intermedius CBS377.75
A. niveoglaucus NRRL128
A. montevidensis CBS491.65T
A. appendiculatus CBS374.75T
A. ruber CBS101748
A. brunneus NRRL133
A. osmophilus CBS134258T
A. proliferans CBS121.45T
A. pseudoglaucus CBS379.75
A. niveoglaucus NRRL137
A. glaucus NRRL117
A. glaucus NRRL121
A. cristatus CBS123.53T
A. costiformis CBS101749T
A. glaucus NRRL120
A. cibarius KACC46765
A. xerophilus NRRL6132
A. sloanii CBS138231
A. niveoglaucus NRRL127T
A. proliferans NRRL114
A. montevidensis NRRL90
A. neocarnoyi NRRL126T
A. megasporus DAOMC250799T
A. ruber CBS530.65T
A. proliferans NRRL62482
A. chevalieri NRRL4755
A. pseudoglaucus CBS101747
A. sloanii CBS138178
A. niveoglaucus NRRL136
Figure 2. One of the most parsimonious trees of Aspergillus sect. Aspergillus based on a combined dataset of ITS, BenA, CaM and RPB2. The tree was rooted to A. xerophilus, A. leucocarpus and A. osmophilus. Support in nodes higher than 80% bootstrap values and 0.95 posterior probabilities are shown above thickened branches. New species are shown in bold and colour, while ex-type strains are followed by T.
A survey of xerophilic Aspergillus from indoor environment... 15
species such as A. proliferans and A. glaucus, A. brunneus and A. niveoglaucus, A. monte-vidensis and A. intermedius, and A. osmophilus and A. xerophilus. On a deeper level, however, the backbones in all gene trees were generally poorly supported, resulting in inconsistent clades among different gene trees. The addition of more newly discovered species of section Aspergillus in future may result in better backbone support. With regards to the new species, A. mallochii was sister to A. appendiculatus, although RPB2 placed it on a unique branch. Aspergillus megasporus resolves in different positions de-pending on gene analyzed, but based on the concatenated phylogeny belongs in a clade with A. brunneus, A. niveoglaucus, A. neocarnoyi, A. glaucus and A. proliferans. For species identifications, it is clear that all three of these genes are superior to ITS and distinguish between all 22 accepted species in sect. Aspergillus.
Extrolites
Aspergillus mallochii and A. megasporus produced several related tryptophan derived al-kaloids including, echinulins, neoechinulins and isoechinulins, but in varying amounts (Table 2). Aspergillus mallochii (DAOMC 146054) was a major producer of neoech-inulin A & B, while also producing isoechinulin A, B & C (Fig. 3a). Quinolactacin A1, A2 & B were among the major extrolites produced by A. megasporus (Fig. 3b). The other was echinulin produced by DAOMC 250799, although it was not detected in DAOMC 250800. The latter strain was generally a poor extrolite producer. The chemical structures of major extrolites produced by A. megasporus and A. mallochii are shown in Fig. 4.
Rel
ativ
e ab
unda
nce
Time (min)
(a)
(b)100
50
0
100
50
0
2.6 2.8 3.0 3.2 3.4 3.6 3.8 4.0 4.2 4.4 4.6 4.8 5.0 5.2 5.4
C19H32O3N2 C 24H 30
O 3N 3
C 39H 43
O 6N 5
C29H37O2N3 C21H44O2
C 24H 30
O 6
C 21H 37
N
C19H21O3N3
neoechinulin A
neoechinulin B
isoechinulin C
quinolactacin
A 2
preechinulin
neoechinulin A
neoechinulin B
echinulinquinolactacin A1
isoechinulin A
isoechinulin B
C20H18O9
Figure 3. Base peak chromatograms observed in positive ionization mode. a Aspergillus mallochii (DAOMC 146054 = KAS 7618) b Aspergillus megasporus (DAOMC 250799 = KAS 6176). Both species show some production of echinulin class of alkaloids to varying amounts. Quinolactacin A1, A2 and B were not detected in A. mallochii.
Cobus M. Visagie et al. / MycoKeys 19: 1–30 (2017)16
Table 2. Overview of the major extrolites detected and product ions.
Extrolite m/z Formula RT (min) Product ions m/zechinulin 462,311 C29H39N3O2 4,16 338,186 266,190 198,128 210,128 270,124isoechinulin A 392,233 C24H29N3O2 3,63 268,108 336,170 256,108 69,071 –isoechinulin B 390,217 C24H27O2N3 3,75 266,092 322,155 334,155 254,092 306,123isoechinulin C 406,212 C24H27O3N3 3,37 334,155 266,092 237,138 338,150 –neoechinulin A 324,171 C19H21O2N3 3,14 256,108 268,108 185,071 69,071 –neoechinulin B 322,155 C19H19O2N3 3,26 254,092 266,095 69,071 226,097 –preechinulin 326,186 C19H23O2N3 2,99 130,065 198,128 270,123 258,124 –quinolactacin A1 271,144 C16H18N2O2 2,66 214,073 – – – –quinolactacin A2 271,144 C16H18N2O2 2,72 214,073 – – – –quinolactacin B 257,129 C15H16N2O2 2,54 214,073 – – – –questin* 283,061 C16H12O5 3,39 268,038 240,042 – – –
* observed in negative ionization mode
echinulinpreechinulin
C5H9 C5H9
H H
R1 R2
isoechinulin Aisoechinulin Bisoechinulin Cneoechinulin Aneoechinulin B
C5H9 CH3
C5H9 CH2
C5H9O CH2
H CH3
H CH2
R1 R2
quinolactacin A1
quinolactacin A2
quinolactacin B
(R) sec-butyl(S) sec-butyli-propyl
R1
Figure 4. Chemical structure of major compounds produced by A. mallochii and A. megasporus.
Taxonomy
Aspergillus mallochii Visagie, Yilmaz & Seifert, sp. nov.MycoBank MB 819025Fig. 5
Etymology. Latin, mallochii, named after Prof. David Malloch, a Canadian specialist in ‘Plectomycetes’ who first collected this species in the 1960’s.
Typus. USA, California, San Mateo, pack rat dung, added to DAOMC in 1969, collected by David Malloch, Holotype DAOM 740296, culture ex-type DAOMC 146054 = CBS 141928 = DTO 357-A5 = KAS 7618.
A survey of xerophilic Aspergillus from indoor environment... 17
Additional material examined. The Netherlands, ‘chocolat miroir’ icing for a cake, unknown date and collector, culture CBS 141776 = DTO 343-G3.
ITS barcode. KX450907. Alternative identification markers: BenA = KX540889, CaM = KX450902, RPB2 = KX450894.
Colony diam, 7 d (in mm), 25 °C. CYA 6–8; CY20S 14–17; MEA 3–4; MEA20S 29–31; DG18 48–50; YES 9–10; M40Y 48–50; MY50G 35–40; MY10-12 29–30; CY20S, DG18, MEA20S at 37 °C no growth; CREA no growth.
Colony characters. CYA: Colonies with restricted growth; conidiophores sparse; cleistothecia absent. CY20S: Colonies grow faster than on CYA; sporulation sparse to moderately dense, greyish to dark green (30E5–F5); cleistothecia dark yellow, abun-dant at colony centre. MEA: Colonies with restricted growth; conidiophores and cle-istothecia absent. MEA20S: Colonies grow faster than on MEA; sporulation sparse, greyish to dark green (30E5–F5); cleistothecia yellow to orange, abundant. DG18: Colonies very fluffy with aerial mycelia giving rise to conidiophores; sporulation sparse to moderately dense, greyish to dark green (30E5–F5); cleistothecia abundant at colo-ny centre, yellow to orange. Homothallic.
Micromorphology on DG18. Cleistothecia eurotium-like, wall consisting of one layer of flattened cells, yellow to orange, turning deep brown with age, glo-bose, 95–250 µm diam. Asci eight-spored, globose, ellipsoidal to pyriform, 10–15 µm diam, maturing after 7–14 d. Ascospores lenticular, equatorial crest present but incomplete, convex surface roughened, 4.5–6 × 3.5–4.5 µm (5.1±0.3 × 3.9±0.3), n = 52. Conidiophores radiate and columnar, uniseriate; stipes smooth, 200–1000 × 7.5–17(–19) µm; vesicle globose, (25–)40–65 µm diam; phialides ampulliform, cov-ering 80–100% of vesicle, 7–11 × 3–5 µm; conidia roughened to spiny, ellipsoidal, connectives easily visible, 4.5–6.5 × 4–5.5 µm (5.4±0.4 × 4.5±0.3), average width/length = 0.83, n = 68.
Extrolites. Isoechinulin A, B & C; neoechinulin A & B; unknowns C20H18O9, C19H32O3N2, C19H21O3N3, C24H30O3N3, C39H43O6N5. Additionally, echinulin, eryth-roglaucin, auroglaucin, flavoglaucin, dihydroauroglaucin, tetrahydroauroglaucin were found in CBS 141776. Some extrolites tentatively identified as tetracyclic compounds were detected in CBS 141776.
Notes. Aspergillus mallochii is phylogenetically and morphologically most similar to A. appendiculatus. Both are unable to grow at 37 °C and both have ascospores with incomplete equatorial furrows. Ascospores of the new species, however, are generally smaller and at least finely roughened compared to the smoother ascospores of A. ap-pendiculatus.
Aspergillus megasporus Visagie, Yilmaz & Seifert, sp. nov.MycoBank MB 819028Fig. 6
Etymology. Latin, megasporus, in reference to the large conidia produced by this species.
Cobus M. Visagie et al. / MycoKeys 19: 1–30 (2017)18
Figure 5. Aspergillus mallochii (DAOMC 146054). a Colonies on MEA, MEA20S, MY10-12 (top row, from left to right), DG18, CY20S, MY50G (bottom row, from left to right) b Texture on DG18 c Asci d Ascospores e Cleistothecium f, g Conidiophores h Conidia. Scale bars: e = 50 µm, c, d, f–h = 10 µm.
A survey of xerophilic Aspergillus from indoor environment... 19
Figure 6. Aspergillus megasporus (DAOMC 250799). a Colonies on MEA, MEA20S, MY10-12 (top row, from left to right), DG18, CY20S, MY50G (bottom row, from left to right) b Texture on DG18 c Asci d Ascospores e Cleistothecium f, g Conidiophores h Conidia. Scale bars: e = 50 µm, c, d, f–h = 10 µm.
Cobus M. Visagie et al. / MycoKeys 19: 1–30 (2017)20
Typus. Canada, Nova Scotia, Wolfville, house dust, 29 January 2015, collected by Allison Walker, isolated by Cobus M. Visagie, holotype DAOM 741781, culture ex-type DAOMC 250799 = CBS 141929= DTO 356-H7 = KAS 6176.
Additional material examined. Canada, New Brunswick, Little Lepreau, house dust, 29 January 2015, collected by Allison Walker, isolated by Cobus M. Visagie, culture DAOMC 250800 = DTO 356-H1 = KAS 5973. The Netherlands, Dutch chocolate butter, August 2007, collected and isolated by Martin Meijer, culture CBS 141772 = DTO 048-I3.
ITS barcode. KX540910. Alternative identification markers: BenA = KX450892, CaM = KX450905, RPB2 = KX450897.
Colony diam, 7 d (in mm), 25 °C. CYA 3–8; CY20S 30–35; MEA 3–5; MEA20S 24–35; DG18 47–50; YES 15–16; M40Y 45–47; MY50G 35–40; MY10-12 40–44; CY20S, DG18, MEA20S at 37 °C no growth, CREA no growth.
Colony characters. CYA: Colonies with restricted growth; conidiophores and cleistothecia absent. CY20S: Colonies grow faster than on CYA; sporulation mod-erately dense, greyish to dark green (30E5–F5); cleistothecia yellow, sparse. MEA: Colonies with restricted growth; conidiophores and cleistothecia absent. MEA20S: Colonies grow faster than on MEA; sporulation moderately dense, greyish to dark green (30E5–F5); cleistothecia yellow, moderately abundant. DG18: Colonies very fluffy with abundant aerial mycelia giving rise to conidiophores; sporulation mod-erately dense, dull to dark green (28E3–F3); cleistothecia abundant, dark yellow to orange. Homothallic.
Micromorphology on DG18. Cleistothecia eurotium-like, wall consisting of one layer of flattened cells, yellow to orange, globose, 115–205 µm diam. Asci eight-spored, globose, ellipsoidal to pyriform, 14–19.5 µm diam. Ascospores lenticular, equatorial crest roughened, convex surface smooth, 5–8 × 3.5–6 µm (6.4±0.6 × 4.9±0.5), n = 51. Conidiophores radiate and columnar, uniseriate; stipes smooth, (30–)60–1000 × (9–)13–20 µm; vesicle globose, (8.5–)20–60 µm diam; phialides ampulliform, cover-ing 70–100% of vesicle, (9–)11–15 × 5–7 µm; conidia roughened to spiny, ellipsoi-dal, connectives often visible, 7–12 × 6–8.5 µm (9.5±1.0 × 6.9±0.5), average width/length = 0.72, n = 85.
Extrolites. Echinulin; neoechinulin A & B; preechinulin; quinolactacin A1 & A2; unknowns C15H20O2, C21H37N, C24H30O6, C29H37O2N3, C21H44O2. In addition, asperflavin, emodin, erythroglaucin, physcion and bisanthron were found in CBS 141772. Some additional extrolites, tentatively identified as tetracyclic compounds, were detected in CBS 141772
Notes. The concatenated phylogeny of BenA, CaM and RPB2 resolves A. megaspo-rus in a clade with A. brunneus, A. niveoglaucus, A. neocarnoyi, A. glaucus and A. prolifer-ans. None of these species are able to grow on CY20S at 37 °C. Aspergillus niveoglaucus and A. megasporus can be distinguished from other species by their large conidia, which are up to 11 and 12 µm in the longest axis respectively. Aspergillus megasporus colonies grow faster than A. niveoglaucus on DG18.
A survey of xerophilic Aspergillus from indoor environment... 21
Discussion
Species of Aspergillus section Aspergillus are xerophilic and widespread in nature. In-door environments, including homes and public buildings, are designed to be as dry as possible, especially in temperate countries, and these conditions select for these xerophiles to thrive. This partially explains the dominance of Aspergillus, Penicillium, Cladosporium and Wallemia in indoor fungal communities (Amend et al. 2010; Flan-nigan and Miller 2011; Samson et al. 2010; Visagie et al. 2014a). In our isolations of xerophiles occurring in Canadian and Hawaiian house dust, these genera were also found to be dominant. Xerophily is spread broadly across Aspergillus. Thirty Aspergillus species were isolated in our survey, excluding the many section Restricti species that will be addressed in another study. All Aspergillus are capable of growth on DG18, but MY10-12 and MY50G have much lower water activities. Species isolated from these selective media included species of sections Aspergillus, Candidi, Flavipedes, Nidulantes, Nigri, Restricti and Versicolores (summarized in Suppl. material 1: Table 1). One new species was discovered from our house dust samples, described as A. megasporus. We also re-identified all cultures from DAOMC deposited as Eurotium. Among these, we discovered an additional species that we described as A. mallochii using morphology, extrolite and phylogenetic analyses.
Aspergillus megasporus was isolated from Canadian house dust collected in Wolfville, Nova Scotia and Little Lepreau, New Brunswick, and was also isolated from chocolate butter in the Netherlands. Phylogenetically, the position of this species varies depend-ing on which gene is analysed; CaM resolves it in its own distinct clade, BenA in a clade with a poorly supported branch with A. glaucus and A. proliferans, and RPB2 closest to A. niveoglaucus. The multigene phylogeny places it in a large clade, including A. brun-neus, A. niveoglaucus, A. neocarnoyi, A. glaucus and A. proliferans. Both A. niveoglaucus and A. megasporus produces conidia respectively reaching 11 and 12 µm, easily distin-guishing them from other species of section Aspergillus. Aspergillus megasporus can be distinguished from A. niveoglaucus based on its faster growth on DG18. Aspergillus megasporus produces extrolites commonly detected in species of section Aspergillus, in-cluding echinulin, neoechinulin and preechinulin. However, we also detected quino-lactacin, a first report for the group. In an independent study using different methods and media, compounds detected from CBS 141772 include asperflavin, auroglaucin, bisanthrons, dihydroauroglaucin, echinulin, emodin, erythroglaucin, flavoglaucin, isoechinulins, neoechinulins, preechinulin, physcion, quinolactacin, tetracyclic com-pounds, and tetrahydroauroglaucin (Frisvad, personal communication).
Aspergillus mallochii was isolated from pack rat dung collected from San Mateo, California, USA. An additional strain was recently isolated from ‘Chocolat miroir’ icing for a cake in the Netherlands. Phylogenetically, it has A. appendiculatus as sister spe-cies, originally described by Blaser (1975) from German smoked sausages. These two species share identical ITS sequences that are distinct from all others in the section (Fig. 2). All other genes, especially RPB2, easily distinguish the two. Morphologically
Cobus M. Visagie et al. / MycoKeys 19: 1–30 (2017)22
they are also similar, but the roughened ascospores of A. mallochii are distinct from the smoother ascospores of A. appendiculatus. In an independent study using different methods and media, compounds detected from CBS 141776 included auroglaucin, dihydroauroglaucin, echinulins, erythroglaucin, flavoglaucin, isoechinulins, neoechi-nulins, tetracyclic compounds and tetrahydroauroglaucin. Comparisons revealed that A. appendiculatus produced several compounds not observed in A. mallochii, such as asperflavin, asperentins, bisanthrons, 5-farnesyl-5,7-dihydroxy-4-methylphthalide, mycophenolic acid, physcion and questin (Nielsen et al. 2011). None of the extrolites identified in A. mallochii are unique to the species.
Quinolactacin A1, A2 & B were the major compounds produced by A. megasporus, the only species of section Aspergillus that produces these. These quinolone structures with a γ-lactam ring were first characterized from fermentations of an unknown Peni-cillium species (Kakinuma et al. 2000; Takahashi et al. 2000) and further characterized by Kim et al. (2001) in Penicillium citrinum, where they were demonstrated to be acetylcholinesterase inhibitors. Quinolactacins have since been reported from mul-tiple Penicillium species from sections Citrina (Houbraken et al. 2011), Brevicompacta (Frisvad et al. 2013; Perrone et al. 2015) and Robsamsonia (Houbraken et al. 2016); Aspergillus quadricinctus, A. stramenius (section Fumigati) (Frisvad and Larsen 2015b; Samson et al. 2007), A. karnatakaensis (section Aenei) (Varga et al. 2010); and from the distantly related marine derived Xylariaceae (Nong et al. 2014). Based on current know-ledge, the echinulins (including echinulin, neoechinulin and isoechinulin) detected in both A. megasporus and A. mallochii seem specific to Aspergillus sections Aspergillus and Restricti (Frisvad and Larsen 2015a). Echinulin was first discovered in A. brunneus (= E. echinulatum) by Quilico and Panizzi (1943). It was subsequently detected in many more section Aspergillus species (Ali et al. 1989; Almeida et al. 2010; Greco et al. 2015; Li et al. 2008b; Slack et al. 2009; Smetanina et al. 2007; Vesonder et al. 1988) and shown to be toxic to animal cells (Ali et al. 1989; Umeda et al. 1974), while swine and mice respectively refused feed and water containing echinulin (Vesonder et al. 1988). The presence of echinulin in the environment is not well documented however. In contrast to the negative effects of echinulin, neoechinulin has anti-oxidant properties (Yagi and Doi 1999) and protected PC12 cell lines, used in neurological research, against cell death by peroxynitrite (Kimoto et al. 2007; Maruyama et al. 2004).
Visagie et al. (2014a) emphasized that despite the existence of comprehensive ITS barcode reference databases, this marker is insufficient for identifying most Aspergil-lus, Penicillium and Talaromyces to species level in culture-independent surveys such as those of Amend et al. (2010) and Adams et al. (2013a; 2013b). The reference sets include sequences for multiple genes obtained from ex-type cultures for all accepted species in these genera (Samson et al. 2014; Visagie et al. 2014b; Yilmaz et al. 2014) and are invaluable as anchoring points for species. Curating databases is laborious and has many complications, but both UNITE and NCBI have ongoing curation projects involving ITS barcodes (Kõljalg et al. 2013; Nilsson et al. 2015; Schoch et al. 2014). ITS will always have limited resolution for species identification. In Aspergillus and Penicillium, ITS is highly conserved in many sections, as is observed in our phylogeny
A survey of xerophilic Aspergillus from indoor environment... 23
of section Aspergillus (Fig. 2). Barcode-based metagenomic studies commonly use Last Common Ancestor (LCA) analyses for assigning OTU’s to GenBank taxonomic nodes. In LCA, when the analysis cannot identify an operational taxonomic unit (OTU) at a taxonomic rank, it will move up one level until it can make a confident assignment. As now implemented, most species of sect. Aspergillus species would be identified only to the generic level. For species-rich genera such as Aspergillus and Penicillium, this is problematic. Different ecologies, functions, extrolites etc. are often associated with specific groups (i.e. true xerophily in at least three sections of Aspergillus), and much potentially important information is lost because of this imprecision. To circumvent this problem, a few recent studies have used alternative genes combined with next generation sequencing (NGS) for making “mass” identifications in Aspergillus. Lee and Yamamoto (2015) assessed the accuracy of high-throughput amplicon sequen-cing using ITS, BenA and CaM, and identified OTU’s using the ex-type sequences published by Samson et al. (2014). Results were promising with both BenA and CaM, which are obviously more accurate than ITS. Unfortunately, amplifications of these alternative barcodes were sometimes problematic, perhaps because they are single copy genes or undocumented sequence variation, especially considering comparisons to only ex-type sequences. Similar results were obtained in a subsequent study by Lee et al. (2016). Even though these types of studies are promising, considerable opti-misation is required to amplify and sequence low copy markers from a complex matrix, and shotgun sequencing may be more effective. No matter what the experimental ap-proach used by ecologists, taxonomists need to make identifications as easy as possible, not only in the traditional morphological sense, but also by generating reference data that will enhance the robustness of analyses of data generated using new technologies such as NGS. Surveys such as ours are thus important not only for discovering previ-ously unnamed species, but for providing more reference sequences in public databases that capture infraspecies sequence variation for multiple barcodes.
Recently, the International Code of Nomenclature for algae fungi and plants (ICN, Melbourne Code; (McNeill et al. 2012)) adopted single name nomenclature for pleomorphic fungi, meaning decisions are needed to choose either the teleomorph-ic (sexual morph) or anamorphic (asexual morph) name to represent the genus. In anticipation of this change, Houbraken and Samson (2011) reviewed the taxonomy and phylogeny Trichocomaceae, of which Penicillium and Aspergillus are the largest groups, using a four gene combined analysis. The situation with the generic concept and name for Aspergillus is complicated and controversial, partly because of conflicting interpretations of phylogenies, and partly because of differing opinions on how much taxonomic weight to apply to sexual states in generic concepts (Houbraken and Sam-son 2011; Pitt and Taylor 2014; Taylor et al. 2016). In this paper, we have followed the traditional broad concept of Aspergillus advocated by the International Commis-sion of Penicillium and Aspergillus (ICPA), which includes species formerly classified in the sexual genera Eurotium, Emericella, Neosartorya and Petromyces in Aspergillus. The section of Aspergillus that is the focus of our paper includes the type species of both Aspergillus (A. glaucus) and Eurotium (E. herbariorum). With the community decision
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to respect the priority of Aspergillus in both the nomenclatural and practical sense, the new species described here would be described in Aspergillus whether a broad or nar-row generic concept is applied. The recent proposal by Taylor et al. (2016) to conserve Aspergillus with the type species changed to A. niger is still being discussed, but at this time seems unlikely to be accepted. If the proposal is implemented, along with the nar-rower generic concept endorsed by these authors, approximately 180 Aspergillus species would be renamed, including those described in this paper.
Acknowledgements
This research was supported by a grant from the Alfred P. Sloan Foundation Program on the Microbiology of the Built Environment. We thank our dust collectors, Allison Walker, Bryce Kendrick and Anthony Amend.
References
Adams RI, Miletto M, Taylor JW, Bruns TD (2013a) Dispersal in microbes: fungi in indoor air are dominated by outdoor air and show dispersal limitation at short distances. The ISME Journal 7: 1262–1273. https://doi.org/10.1038/ismej.2013.28
Adams RI, Miletto M, Taylor JW, Bruns TD (2013b) The diversity and distribution of fungi on residential surfaces. PLoS ONE 8: e78866. https://doi.org/10.1371/journal.pone.0078866
Ali M, Mohammed N, Alnaqeeb MA, Hassan RA, Ahmad HS (1989) Toxicity of echinu-lin from Aspergillus chevalieri in rabbits. Toxicology Letters 48: 235–241. https://doi.org/10.1016/0378-4274(89)90049-0
Almeida A, Dethoup T, Singburaudom N, Lima R, Vasconcelos MH, Pinto M, Kijjoa A (2010) The in vitro anticancer activity of the crude extract of the sponge-associated fungus Eurotium cristatum and its secondary metabolites. Journal of Natural Pharmaceuticals 1: 25–29. https://doi.org/10.4103/2229-5119.73583
Amend AS, Seifert KA, Samson RA, Bruns TD (2010) Indoor fungal composition is geo-graphically patterned and more diverse in temperate zones than in the tropics. PNAS 107: 13748–13753. https://doi.org/10.1073/pnas.1000454107
Bachmann M, Luthy J, Schlatter C (1979) Toxicity and mutagenicity of molds of the Asper-gillus glaucus group, identification of physcion and three related anthraquinones as main toxic constituents from Aspergillus chevalieri. Journal of Agriculture and Food Chemistry 27: 1342–1347. https://doi.org/10.1021/jf60226a021
Blaser P (1975) Taxonomische und physiologische Untersuchungen über die Gatung Eurotium Link ex Fries. Sydowia 28: 1–49. https://doi.org/10.3929/ethz-a-000077128
Cavka M, Glasnović A, Janković I, Sikanjić P, Perić B, Brkljacić B, Mlinarić-Missoni E, Skrlin J (2010) Microbiological analysis of a mummy from the archeological museum in Zagreb. Collegium Antropologicum 34: 803–805
A survey of xerophilic Aspergillus from indoor environment... 25
Cole RJ, Cox RH (1981) Tremorgen Group. In: Cole RJ, Cox RH (Eds) Handbook of Toxic Fungal Metabolites. Academic Press, San Diego, 355–509. https://doi.org/10.1016/B978-0-12-179760-7.50013-9
Collado J, Platas G, Paulus B, Bills GF (2007) High-throughput culturing of fungi from plant litter by a dilution-to-extinction technique. FEMS Microbiology Ecology 60: 521–533. https://doi.org/10.1111/j.1574-6941.2007.00294.x
de Hoog GS, Gerrits van den Ende AH (1998) Molecular diagnostics of clinical strains of filamen-tous Basidiomycetes. Mycoses 41: 183–189. https://doi.org/10.1111/j.1439-0507.1998.tb00321.x
de Hoog GS, Guarro J, Gene J, Figueras MJ (2014) Atlas of Clinical Fungi. CBS-KNAW Fungal Biodiversity Centre, Utrecht, the Netherlands, 1126 pp.
Flannigan B, Miller JD (2011) Microbial growth in indoor environments. In: Flannigan B, Samson RA, Miller JD (Eds) Microorganisms in Home and Indoor Work Environments: Diversity, Health Impacts, Investigation and Control. CRC Press, London, 57–108. htt-ps://doi.org/10.1201/b10838-5
Frisvad JC, Houbraken J, Popma S, Samson RA (2013) Two new Penicillium species Penicillium buchwaldii and Penicillium spathulatum, producing the anticancer compound asperphena-mate. FEMS Microbiology Letters 339: 77–92. https://doi.org/10.1111/1574-6968.12054
Frisvad JC, Larsen TO (2015a) Chemodiversity in the genus Aspergillus. Applied Microbiology and Biotechnology 99: 7859–7877. https://doi.org/10.1007/s00253-015-6839-z
Frisvad JC, Larsen TO (2015b) Extrolites of Aspergillus fumigatus and other pathogenic spe-cies in Aspergillus section Fumigati. Frontiers in Microbiology 6: 1485. https://doi.org/10.3389/fmicb.2015.01485
Frisvad JC, Thrane U (1987) Standardized High Performance Liquid Chromatography of 182 mycotoxins and other fungal metabolites based on alkylphenone indices and UV VIS spectra (diode array detection). Journal of Chromatography 404: 195–214. https://doi.org/10.1016/S0021-9673(01)86850-3
Glass NL, Donaldson GC (1995) Development of premier sets designed for use with the PCR to amplify conserved genes from filamentous Ascomycetes. Applied and Environmental Microbiology 61: 1323–1330
Gomes NM, Dethoup T, Singburaudom N, Gales L, Silva AMS, Kijjoa A (2012) Euroc-ristatine, a new diketopiperazine dimer from the marine sponge-associated fungus Eu-rotium cristatum. Phytochemistry Letters 5: 717–720. https://doi.org/10.1016/j.phy-tol.2012.07.010
Greco M, Kemppainen M, Pose G, Pardo A (2015) Taxonomic characterization and secondary metabolite profiling of Aspergillus section Aspergillus contaminating feeds and feedstuffs. Toxins 7: 3512–3537. https://doi.org/10.3390/toxins7093512
Green BJ, Tovey ER, Sercombe JK, Blachere FM, Beezhold DH, Schmechel D (2006) Air-borne fungal fragments and allergenicity. Medical Mycology 44: S245–255. https://doi.org/10.1080/13693780600776308
Harrold CE (1950) Studies in the genus Eremascus. I. The rediscovery of Eremascus albus Eidam and some new observations concerning its life-history and cytology. Annals of Botany 14: 127–148.
Cobus M. Visagie et al. / MycoKeys 19: 1–30 (2017)26
Hocking AD, Pitt JI (1980) Dichloran-glycerol medium for enumeration of xerophilic fungi from low-moisture foods. Applied and Environmental Microbiology 39: 488–492.
Hong S-B, Cho H-S, Shin H-D, Frisvad JC, Samson RA (2006) Novel Neosartorya species isolated from soil in Korea. International Journal of Systematic and Evolutionary Microbi-ology 56: 477–486. https://doi.org/10.1099/ijs.0.63980-0
Houbraken J, Frisvad JC, Samson RA (2011) Taxonomy of Penicillium section Citrina. Stud Mycol 70: 53–138. https://doi.org/10.3114/sim.2011.70.02
Houbraken J, Samson RA (2011) Phylogeny of Penicillium and the segregation of Trichoco-maceae into three families. Stud Mycol 70: 1–51. https://doi.org/10.3114/sim.2011.70.01
Houbraken J, Wang L, Lee HB, Frisvad JC (2016) New sections in Penicillium containing novel species producing patulin, pyripyropens or other bioactive compounds. Persoonia 36: 299–314. https://doi.org/10.3767/003158516x692040
Hubka V, Kolarik M, Kubátová A, Peterson SW (2013) Taxonomic revision of Eurotium and transfer of species to Aspergillus. Mycologia 105: 912–937. https://doi.org/10.3852/12-151
Hubka V, Kubátová A, Mallátová N, Sedlacek P, Melichar J, Magdalena S, Mencl K, Lysková P, Sramkova B, Chudíčková M, Hamal P, Kolarik M (2012) Rare and new etiological agents revealed among 178 clinical Aspergillus strains obtained from Czech patients and characterized by molecular sequencing. Medical Mycology 50: 601–610. https://doi.org/10.3109/13693786.2012
Kakinuma N, Iwai H, Takahashi S, Hamano K, Yanagisawa T, Nagai K, Tanaka K, Suzuki K, Kirikae F, Kirikae T, Nakagawa A (2000) Quinolactacins A, B and C: Novel quinolone com-pounds from Penicillium sp. EPF-6. I. Taxonomy, production, isolation and biological proper-ties. The Journal of Antibiotics 53: 1247–1251. https://doi.org/10.7164/antibiotics.53.1247
Kanokmedhakul K, Kanokmedhakul S, Suwannatrai R, Soytong K, Prabpai S, Kongsaeree P (2011) Bioactive meroterpenoids and alkaloids from the fungus Eurotium chevalieri. Tet-rahedron 67: 5461–5468. https://doi.org/10.1016/j.tet.2011.05.066
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: im-provements in performance and usability. Molecular Biology and Evolution 30: 772–780. https://doi.org/10.1093/molbev/mst010
Kim W-G, Song N-K, Yoo I-D (2001) Quinolactacins A1 and A2, new actylcholinesterase inhibitors from Penicillium citrinum. The Journal of Antibiotics 54: 831–835.
Kimoto K, Aoki T, Shibata Y, Kamisuki S, Sugawara F, Kuramochi K, Nakazaki A, Kobatashi S, Kuroiwa K, Watanabe N, Arai T (2007) Structure-activity relationships of neoechinulin A analogues with cytoprotection against peroxynitrite-induced PC12 cell death. The Jour-nal of Antibiotics 60: 614–621. https://doi.org/10.1038/ja.2007.79
Kõljalg U, Nilsson RH, Abarenkov K, Tedersoo L, Taylor AFS, Bahram M, Bates ST, Bruns TD, Bengtsson-Palme J, Callaghan TM, Douglas B, Drenkhan T, Eberhardt U, Dueñas M, Grebenc T, Griffith GW, Hartmann M, Kirk PM, Kohout P, Larsson E, Lindahl BD, Lücking R, Martín MP, Matheny PB, Nguyen NH, Niskanen T, Oja J, Peay KG, Peintner U, Peterson M, Põldmaa K, Saag L, Saar I, Schüßler A, Scott JA, Senés C, Smith ME, Suija A, Taylor DL, Telleria MT, Weiss M, Larsson K-H (2013) Towards a unified paradigm for sequence-based identification of fungi. Molecular Ecology Resources 22: 5271–5277. https://doi.org/10.1111/mec.12481
A survey of xerophilic Aspergillus from indoor environment... 27
Kornerup A, Wanscher JH (1967) Methuen Handbook of Colour. Methuen & Co Ltd, 243 pp.Lee S, An C, Xu S, Lee S, Yamamoto N (2016) High-throughput sequencing reveals unprec-
edented diversities of Aspergillus species in outdoor air. Letters in Applied Microbiology 63: 165–171. https://doi.org/10.1111/lam.12608
Lee S, Yamamoto N (2015) Accuracy of the high-throughput amplicon sequencing to iden-tify species within the genus Aspergillus. Fungal Biology 119: 1311–1321. https://doi.org/10.1016/j.funbio.2015.10.006
Li DL, Li XM, Li TG, Dang HY, Proksch P, Wang BG (2008a) Benzaldehyde derivatives from Eurotium rubrum, an endophytic fungus derived from the mangrove plant Hibiscus tiliaceus. Chemical and Pharmaceutical Bulletin 56: 1282–1285. https://doi.org/10.1248/cpb.56.1282
Li DL, Li XM, Li TG, Dang HY, Wang BG (2008b) Dioxopiperazine alkaloids produced by the marine mangrove derived endophytic fungus Eurotium rubrum. Helvetica Chimica Acta 91: 1888–1893.
Liu YJ, Whelen S, Hall BD (1999) Phylogenetic relationships among Ascomycetes: evidence from an RNA polymerse II subunit. Molecular Biology and Evolution 16: 1799–1808. https://doi.org/10.1093/oxfordjournals.molbev.a026092
Maruyama K, Ohuchi T, Yoshida K, Shibata Y, Sugawara F, Arai T (2004) Protective prop-erties of neoechinulin A against SIN-1-induced neuronal cell death. The Journal of Bio-chemistry 136: 81–87. https://doi.org/10.1093/jb/mvh103
Masclaux F, Guého E, de hoog GS, Christen R (1995) Phylogenetic relationships of hu-man-pathogenic Cladosporium (Xylohypha) species inferred from partial LS rRNA se-quences. Journal of Medical and Veterinary Mycology 33: 327–338. https://doi.org/10.1080/02681219580000651
McNeill J, Barrie FR, Buck WR, Demoulin V, Greuter W, Hawksworth DL, Herendeen PS, Knapp S, Marhold K, Prado J, Prud’homme van Reine W, Smith G, Wiersema JH, Mem-bers, Turland NJ (2012) International Code of Nomenclature for algae, fungi and plants (Melbourne Code). Koeltz Scientific Books, Konigstein. [Regnum vegetabile no. 154]
Micheluz A, Manente S, Tigini V, Prigione V (2015) The extreme environment of a library: Xerophilic fungi inhabiting indoor niches. International Biodeterioration & Biodegrada-tion 99: 1–7. https://doi.org/10.1016/j.ibiod.2014.12.012
Nazar M, Ali M, Fatima T, Gubler CJ (1984) Toxicity of flavoglaucin from Aspergillus chevalieri in rabbits. Toxicology Letters 23: 233–237. https://doi.org/10.1016/0378-4274(84)90132-2
Nielsen KF, Mansson M, Rank C, Frisvad JC, Larsen TO (2011) Dereplication of micro-bial natural products by LC-DAD-TOFMS. Journal of Natural Products 74: 2338–2348. https://doi.org/10.1021/np200254t
Nilsson RH, Tedersoo L, Ryberg M, Kristiansson E, Hartmann M, Unterseher M, M Porter T, Bengtsson-Palme J, M Walker D, de Sousa F, Andres Gamper H, Larsson E, Lars-son K-H, Kõljalg U, C Edgar R, Abarenkov K (2015) A comprehensive, automatically updated fungal its sequence dataset for reference-based chimera control in environmental sequencing efforts. Microbes and Environments 30: 145–150. https://doi.org/10.1264/jsme2.ME14121
Cobus M. Visagie et al. / MycoKeys 19: 1–30 (2017)28
Nong XH, Zhang XY, Xu XY, Sun YL, Qi SH (2014) Alkaloids from Xylariaceae sp., a marine-derived fungus. Natural Product Communications 9: 467–468.
Nylander AJJ (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.
Perrone G, Samson RA, Frisvad JC, Susca A, Gunde-Cimerman N, Epifani F, Houbraken J (2015) Penicillium salamii, a new species occurring during seasoning of dry-cured meat. International Journal of Food Microbiology 193: 91–98. https://doi.org/10.1016/j.ijfood-micro.2014.10.023
Peterson SW (2008) Phylogenetic analysis of Aspergillus species using DNA sequences from four loci. Mycologia 100: 205–226. https://doi.org/10.3852/mycologia.100.2.205
Peterson SW, Vega F, Posada F, Nagai C (2005) Penicillium coffeae, a new endophytic species isolated from a coffee plant and its phylogenetic relationship to P. fellutanum, P. thiersii and P. brocae based on parsimony analysis of multilocus DNA sequences. Mycologia 97: 659–666.
Pinar G, Piombino-Mascali D, Maixner F, Zink A, Sterflinger K (2013) Microbial survey of the mummies from the Capuchin Catacombs of Palermo, Italy: biodeterioration risk and contamination of the indoor air. FEMS Microbiology Ecology 86: 341–356. https://doi.org/10.1111/1574-6941.12165
Pinar G, Tafer H, Sterflinger K, Pinzari F (2015) Amid the possible causes of a very famous foxing: molecular and microscopic insight into Leonardo da Vinci’s self-portrait. Envi-ronmental Microbiology Reports 7: 849–859. https://doi.org/10.1111/1758-2229.12313
Pitt JI (1975) Xerophilic fungi and the spoilage of foods of plant origin. In: Duckworth RB (Ed.) Water relations of foods. Academic Press, London, 273–307.
Pitt JI, Hocking AD (2009) Fungi and Food Spoilage. Springer, Dordrecht. https://doi.org/10.1007/978-0-387-92207-2
Pitt JI, Taylor JW (2014) Aspergillus, its sexual states and the new International Code of Nomen-clature. Mycologia 106: 1051–1062. https://doi.org/10.3852/14-060
Quilico A, Panizzi L (1943) Chemische Untersuchungen über Aspergillus echinulatus, I. Mitteilung. Berichte der deutschen chemischen Gesellschaft 76: 348–358. https://doi.org/10.1002/cber.19430760408
Rabie CJ, De Klerk WA, Terblanche M (1964) Toxicity of Aspergillus amstelodami to poultry and rabbits. South African Journal of Agricultural Science 7: 341–344.
Raper KB, Fennell DI (1965) The genus Aspergillus. Williams & Wilkins Company, Baltimore, 686 pp.
Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) Mrbayes 3.2: Efficient bayesian phylogenetic in-ference and model choice across a large model space. Systematic Biology 61: 539–542. https://doi.org/10.1093/sysbio/sys029
Samson RA, Hong S, Peterson SW, Frisvad JC, Varga J (2007) Polyphasic taxonomy of Asper-gillus section Fumigati and its teleomorph Neosartorya. Studies in Mycology 59: 147–203. https://doi.org/10.3114/sim.2007.59.14
Samson RA, Houbraken J, Thrane U, Frisvad JC, Andersen B (2010) Food and Indoor Fungi. CBS Laboratory manual, 390 pp.
A survey of xerophilic Aspergillus from indoor environment... 29
Samson RA, Visagie CM, Houbraken J, Hong S-B, Hubka V, Klaassen CHW, Perrone G, Seifert KA, Susca A, Tanney JB, Varga J, Kocsube S, Szigeti G, Yaguchi T, Frisvad JC (2014) Phylogeny, identification and nomenclature of the genus Aspergillus. Studies in Mycology 78: 141–173. https://doi.org/10.1016/j.simyco.2014.07.004
Schoch CL, Robbertse B, Robert V, Vu D, Cardinali G, Irinyi L, Meyer W, Nilsson RH, Hughes K, Miller AN, Kirk PM, Abarenkov K, Aime MC, Ariyawansa HA, Bidartondo M, Boekhout T, Buyck B, Cai Q, Chen J, Crespo A, Crous PW, Damm U, De Beer ZW, Dentinger BTM, Divakar PK, Dueñas M, Feau N, Fliegerova K, García MA, Ge Z-W, Griffith GW, Groenewald JZ, Groenewald M, Grube M, Gryzenhout M, Gueidan C, Guo L, Hambleton S, Hamelin R, Hansen K, Hofstetter V, Hong S-B, Houbraken J, Hyde KD, Inderbitzin P, Johnston PR, Karunarathna SC, Kõljalg U, Kovács GM, Krai-chak E, Krizsan K, Kurtzman CP, Larsson K-H, Leavitt S, Letcher PM, Liimatainen K, Liu J-K, Lodge DJ, Jennifer Luangsa-Ard J, Lumbsch HT, Maharachchikumbura SSN, Manamgoda D, Martín MP, Minnis AM, Moncalvo J-M, Mulè G, Nakasone KK, Nis-kanen T, Olariaga I, Papp T, Petkovits T, Pino-Bodas R, Powell MJ, Raja HA, Redecker D, Sarmiento-Ramirez JM, Seifert KA, Shrestha B, Stenroos S, Stielow B, Suh S-O, Tan-aka K, Tedersoo L, Telleria MT, Udayanga D, Untereiner WA, Diéguez Uribeondo J, Subbarao KV, Vágvölgyi C, Visagie C, Voigt K, Walker DM, Weir BS, Weiss M, Wijaya-wardene NN, Wingfield MJ, Xu JP, Yang ZL, Zhang N, Zhuang W-Y, Federhen S (2014) Finding needles in haystacks: linking scientific names, reference specimens and molecular data for Fungi. Database (Oxford) 2014: 1–21. https://doi.org/10.1093/database/bau061
Schoch CL, Seifert KA, Huhndorf S, Robert V, Spouge JL, Levesque CA, Chen W (2012) Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi PNAS 109: 6241–6246. https://doi.org/10.1073/pnas.1117018109/-/DCSupplemental
Scott WJ (1957) Water Relations of Food Spoilage Microorganisms. Advances in Food Re-search 7: 83–127. https://doi.org/10.1016/S0065-2628(08)60247-5
Semeniuk G, Harshfield GS, Carlson CW, Hesseltine CW, Kwolek WF (1971) Mycotoxins in Aspergillus. Mycopathologia et Mycologia Applicata 43: 137–152. https://doi.org/10.1007/BF02051714
Slack GJ, Puniani E, Frisvad JC, Samson RA, Miller JD (2009) Secondary metabolites from Eurotium species, Aspergillus calidoustus and A. insuetus common in Canadian homes with a review of their chemistry and biological activities. Mycological Research 113: 480–490. https://doi.org/10.1016/j.mycres.2008.12.002
Smetanina OF, Kalinovski AI, Khudyakova YV, Slinkina NN, Pivkin MV, Kuznetsova TA (2007) Metabolites from the marine fungus Eurotium repens. Chemistry of Natural Com-pounds 43: 395–398. https://doi.org/10.1007/s10600-007-0147-5
Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Massachusetts.
Takahashi S, Kakinuma N, Iwai H, Yanagisawa T, Nagai K, Suzuki K, Tokunaga T, Nakagawa A (2000) Quinolactacins A, B and C: Novel quinolone compounds from Penicillium sp. EPF-6. II. Physico-chemical properties and structure elucidation. The Journal of Antibiotics 53: 1252–1256. https://doi.org/10.7164/antibiotics.53.1252
Cobus M. Visagie et al. / MycoKeys 19: 1–30 (2017)30
Taylor JW, Göker M, Pitt JI (2016) Choosing one name for pleomorphic fungi: The example of Aspergillus versus Eurotium, Neosartorya and Emericella. Taxon 65: 593–601. https://doi.org/10.12705/653.10
Thom C, Raper KB (1941) The Aspergillus glaucus group. United States Department of Agri-culture 426: 1–46.
Umeda M, Yamashita T, Saito M, Sekita S, Takahashi C (1974) Chemical and cytotoxicity survey on the metabolites of toxic fungi. The Japan Journal of Experimental Medicine 44: 83–96.
Varga J, Frisvad JC, Samson RA (2010) Aspergillus sect. Aeni sect. nov., a new section of the ge-nus for A. karnatakaensis sp. nov. and some allied fungi. IMA Fungus 1: 197–205. https://doi.org/10.5598/imafungus.2010.01.02.13
Vesonder RF, Lambert R, Wicklow DT, Biehl ML (1988) Eurotium spp. and echinulin in feed refused by swine. Applied and Environmental Microbiology 54: 830–831.
Visagie CM, Hirooka Y, Tanney JB, Whitfield E, Mwange K, Meijer M, Amend AS, Seif-ert KA, Samson RA (2014a) Aspergillus, Penicillium and Talaromyces isolated from house dust samples collected around the world. Studies in Mycology 78: 63–139. https://doi.org/10.1016/j.simyco.2014.07.002
Visagie CM, Houbraken J, Frisvad JC, Hong S-B, Klaassen CHW, Perrone G, Seifert KA, Varga J, Yaguchi T, Samson RA (2014b) Identification and nomenclature of the genus Penicillium. Studies in Mycology 78: 343–371. https://doi.org/10.1016/j.simyco.2014.09.001
Visagie CM, Renaud JB, Burgess KMN, Malloch D, Clark D, Ketch L, Urb M, Louis-Seize G, Assabgui R, Sumarah MW, Seifert KA (2016) Fifteen new species of Penicillium. Persoo-nia 36: 247–280. https://doi.org/10.3767/003158516X691627
Yagi R, Doi M (1999) Isolation of an antioxidative substance produced by Aspergillus repens. Bio-science, Biotechnology, and Biochemistry 63: 932–933. https://doi.org/10.1271/bbb.63.932
Yilmaz N, Visagie CM, Houbraken J, Frisvad JC, Samson RA (2014) Polyphasic taxonomy of the genus Talaromyces. Studies in Mycology 78: 175–341. https://doi.org/10.1016/j.simy-co.2014.08.001
Supplementary material 1
Species isolated from house dust using selective xerophilic mediaAuthors: Cobus M. Visagie, Neriman Yilmaz, Justin B. Renaud, Mark W. Sumarah, Vit Hubka, Jens C. Frisvad, Amanda J. Chen, Martin Meijer, Keith A. SeifertData type: Occurrence, GenBank infoExplanation note: Species isolated from house dust using selective xerophilic media,
their occurrence and GenBank numbers for sequences generated for these strains.Copyright notice: This dataset is made available under the Open Database License
(http://opendatacommons.org/licenses/odbl/1.0/). The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
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